Abstract
As is the case with most hair-cell organs, the vestibular labyrinth receives a dual innervation. Afferent nerve fibers arise from bipolar cells in the vestibular (Scarpa’s) ganglion. The peripheral process of each ganglion cell gets synaptic inputs from hair cells in one of several discrete organs, and its central process conveys the resulting information, encoded in the spacing of action potentials, to the vestibular nuclei and the cerebellum. In addition, hair cells and afferent nerve terminals are innervated by efferent fibers originating in the brain stem and reaching the periphery by way of the vestibular nerve. This chapter reviews our understanding of the efferent vestibular system (EVS), including its neuroanatomical organization, candidate neurotransmitters, peripheral actions on afferent discharge as revealed by electrical stimulation of EVS pathways, and the underlying cellular (synaptic) and neurotransmitter mechanisms. To consider possible functions of the EVS, the chapter then describes the vestibular and nonvestibular signals carried by efferent neurons and how these signals might modify the information carried by afferents. Though our emphasis is on the mammalian EVS, results in nonmammalian species are also considered, as these provide insights into efferent function.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19–29
Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73–120
Almanza A, Navarrete F, Vega R, Soto E (2007) Modulation of voltage-gated Ca2+ current in vestibular hair cells by nitric oxide. J Neurophysiol 97:1188–1195
Anderson AD, Troyanovskaya M, Wackym PA (1997) Differential expression of alpha2–7, alpha9 and beta2–4 nicotinic acetylcholine receptor subunit mRNA in the vestibular end organs and Scarpa’s ganglia of the rat. Brain Res 778:409–413
Andrianov GN, Ryzhova IV (1999) Opioid peptides as possible neuromodulators of the afferent synaptic transmission in the frog semicircular canal. Neuroscience 93:801–806
Annoni JM, Cochran SL, Precht W (1984) Pharmacology of the vestibular hair cell-afferent fiber synapse in the frog. J Neurosci 4:2106–2116
Art JJ, Fettiplace R, Fuchs PA (1984) Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J Physiol 356:525–550
Ashmore JF, Russell IJ (1982) Effects of efferent nerve stimulation on hair cells of the frog sacculus. J Physiol 329:25P–26P
Aubert A, Norris CH, Guth PS (1994) Influence of ATP and ATP agonists on the physiology of the isolated semicircular canal of the frog (Rana pipiens). Neuroscience 62:963–974
Aubert A, Norris CH, Guth PS (1995) Indirect evidence for the presence and physiological role of endogenous extracellular ATP in the semicircular canal. Neuroscience 64:1153–1160
Bailey GP, Sewell WF (2000a) Calcitonin gene-related peptide suppresses hair cell responses to mechanical stimulation in the Xenopus lateral line organ. J Neurosci 20:5163–5169
Bailey GP, Sewell WF (2000b) Pharmacological characterization of the CGRP receptor in the lateral line organ of Xenopus laevis. J Assoc Res Otolaryngol 1:82–88
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
Barbas-Henry HA, Lohman AHM (1988) Primary projections and efferent cells of the VIIIth cranial nerve in the monitor lizard, Varanus exanthematicus. J Comp Neurol 277:234–249
Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451–465
Behrend O, Schwark C, Kunihiro T, Strupp M (1997) Cyclic GMP inhibits and shifts the activation curve of the delayed-rectifier (I[K1]) of type I mammalian vestibular hair cells. Neuroreport 8:2687–2690
Bernard C, Cochran SL, Precht W (1985) Presynaptic actions of cholinergic agents upon the hair cell-afferent fiber synapses in the vestibular labyrinth of the frog. Brain Res 338:225–236
Blanks RHI, Precht W (1976) Functional characterization of primary vestibular afferents in the frog. Exp Brain Res 25:369–390
Bobbin RP, Konishi T (1971) Acetylcholine mimics crossed olivocochlear bundle stimulation. Nature 231:222–223
Bobbin RP, Konishi T (1974) Action of cholinergic and anticholinergic drugs at the crossed olivochlear bundle-hair cell junction. Acta Otolaryngol (Stockh) 77:55–65
Bowery NG, Bettler B, Froestl W, Gallagher JP, Marshall F, Raiteri M, Bonner TI, Enna SJ (2002) International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid (B) receptors: structure and function. Pharmacol Rev 54:247–264
Boyle R, Highstein SM (1990a) Resting discharge and response dynamics of horizontal semicircular canal afferents in the toadfish, Opsanus tau. J Neurosci 10:1557–1569
Boyle R, Highstein SM (1990b) Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10:1570–1582
Boyle R, Carey JP, Highstein SM (1991) Morphological correlates of response dynamics and efferent stimulation in horizontal semicircular canal afferents of the toadfish, Opsanus tau. J Neurophysiol 66:1504–1521
Boyle RD, Rabbitt RD, Highstein SM (2009) Efferent control of hair cell and afferent responses in the semicircular canals. J Neurophysiol 102:1513–1525
Brichta AM, Goldberg JM (1996) Afferent and efferent responses from morphological fiber classes in the turtle posterior crista. Ann N Y Acad Sci 781:183–195
Brichta AM, Goldberg JM (2000a) Morphological identification of physiologically characterized afferents innervating the turtle posterior crista. J Neurophysiol 83:1202–1223
Brichta AM, Goldberg JM (2000b) Responses to efferent activation and excitatory response-intensity relations of turtle posterior-crista afferents. J Neurophysiol 83:1224–1242
Brichta AM, Peterson EH (1994) Functional architecture of vestibular primary afferents from the posterior semicircular canal of a turtle, Pseudemys (Trachemys) scripta elegans. J Comp Neurol 344:481–507
Brontë-Stewart HM, Lisberger SG (1994) Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys. J Neurosci 14:1290–1308
Brown DA (1988) M currents: an update. Trends Neurosci 11:294–299
Brown DA, Passmore GM (2009) Neural KCNQ (Kv7) channels. Br J Pharmacol 156:1185–1195
Carpenter MB, Chang L, Pereira AB, Hersch LB, Bruce G, Wu J-Y (1987) Vestibular and cochlear efferent neurons in the monkey identified by immunocytochemical methods. Brain Res 408:275–280
Caulfield MP, Birdsall NJ (1998) International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50:279–290
Chebib M, Johnston GAB (1999) The “ABC” of GABA receptors: a brief review. Clin Exp Pharmacol Physiol 26:937–940
Chen JW, Eatock RA (2000) Major potassium conductance in type I hair cells from rat semicircular canals: characterization and modulation by nitric oxide. J Neurophysiol 84:139–151
Chi FL, Jiao Y, Liu HJ, Wang J, Shi Y, Barr JJ (2007) Retrograde neuron tracing with microspheres reveals projection of CGRP-immunolabeled vestibular afferent neurons to the vestibular efferent nucleus in the brainstem of rats. Neuroendocrinology 85:131–138
Churchill JA, Schuknecht HF, Doran R (1956) Acetylcholinesterase activity in the cochlea. Laryngoscope 66:1–15
Claas B, Fritzsch B, Münz H (1981) Common efferents to lateral line and labyrinthine hair cells in aquatic vertebrates. Neurosci Lett 27:231–235
Connor JA (1978) Slow repetitive activity from fast conductance changes in neurons. Fed Proc 37:2139–2145
Cooper JR, Bloom FE, Roth RH (2002) The biochemical basis of neuropharmacology. Raven Press, New York
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):1–7
Curthoys IS (1982) The response of primary horizontal semicircular canal neurons in the rat and guinea pig to angular acceleration. Exp Brain Res 47:286–294
Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of oculomotor, neural, and oculomotor consequences of unilateral vestibular loss. J Vestib Res 5:67–107
Dawkins R, Keller SL, Sewell WF (2005) Pharmacology of acetylcholine-mediated cell signaling in the lateral line organ following efferent stimulation. J Neurophysiol 93:2541–2551
de Robertis ED, Bennett HS (1955) Some features of the submicroscopic morphology of synapses in frog and earthworm. J Biophys Biochem Cytol 1:47–58
Dechesne C, Raymond J, Sans A (1984) The efferent vestibular system in the cat: a horseradish peroxidase and fluorescent retrograde tracer study. Neuroscience 11:893–901
Delmas P, Brown DA (2005) Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat Rev Neurosci 6:850–862
Derbenev AV, Linn CL, Guth PS (2005) Muscarinic ACh receptor activation causes transmitter release from isolated frog vestibular hair cells. J Neurophysiol 94:3134–3142
Desai SS, Dhaliwal J, Lysakowski A (2004) NOS immunochemical staining in calyces in chinchilla vestibular endorgans. Association for Research in Otolaryngology Midwinter Meeting Abstracts 27:853
Desai SS, Ali H, Lysakowski A (2005a) Comparative morphology of rodent vestibular periphery. II. Cristae ampullares. J Neurophysiol 93:267–280
Desai SS, Zeh C, Lysakowski A (2005b) Comparative morphology of rodent vestibular periphery. I. Saccular and utricular maculae. J Neurophysiol 93:251–266
Desmadryl G, Dechesne CJ (1992) Calretinin immunoreactivity in chinchilla and guinea pig vestibular end organs characterizes the calyx unit subpopulation. Exp Brain Res 89:105–108
Desmedt JE, Monaco P (1961) Mode of action of the efferent olivo-cochlear bundle on the inner ear. Nature 192:1263–1265
Dickman JD, Correia MG (1993) Bilateral communication between vestibular labyrinths in pigeons. Neuroscience 57:1097–1108
Didier A, Dupont J, Cazals Y (1990) GABA immunoreactivity of calyceal nerve endings in the vestibular system of the guinea pig. Cell Tissue Res 260:415–419
Dohlman G, Farkashidy J, Salonna F (1958) Centrifugal nerve fibers to the sensory epithelium of the vestibular labyrinth. J Laryngol 72:984–991
Dowdall MJ, Boyne AF, Whittaker VP (1974) Adenosine triphosphate. A constituent of cholinergic synaptic vesicles. Biochem J 140:1–12
Drescher DG, Kerr TP, Drescher MJ (1999) Autoradiographic demonstration of quinuclidinyl benzilate binding sites in the vestibular organs of the gerbil. Brain Res 845:199–207
Drescher DG, Ramakrishnan NA, Drescher MJ, Chun W, Wang X, Myers SF, Green GE, Sadrazodi K, Karadaghy AA, Poopat N, Karpenko AN, Khan KM, Hatfield JS (2004) Cloning and characterization of alpha9 subunits of the nicotinic acetylcholine receptor expressed by saccular hair cells of the rainbow trout (Oncorhynchus mykiss). Neuroscience 127:737–752
Eglen RM (2005) Muscarinic receptor subtype pharmacology and physiology. Prog Med Chem 43:105–136
Elgoyhen AB, Johnson DS, Boutler J, Vetter DE, Heinemann S (1994) α9: an acetylcholine receptor with novel pharmacological properties expressed in rat chochlear hair cells. Cell 79:705–715
Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heinemann SF, Boulter J (2001) Alpha10, a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci U S A 98:3501–3506
Engström H (1958) On the double innervation of the sensory epithelia of the inner ear. Acta Otolaryngol (Stockh) 49:109–118
Engström H, Wersäll J (1958) The ultrastructural organization of the organ of Corti and of the vestibular sensory epithelia. Exp Cell Res 5:460–492
Eybalin M (1993) Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73:309–373
Ezure K, Cohen MS, Wilson VJ (1983) Response of cat semicircular canal afferents to sinusoidal polarizing currents: implications for input-output properties of second-order neurons. J Neurophysiol 49:639–648
Favre D, Sans A (1979) Morphological changes in afferent vestibular hair cell synapses during the postnatal development of the cat. J Neurocytol 8:765–775
Fernández C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39:996–1008
Fernández C, Baird RA, Goldberg JM (1988) The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals. J Neurophysiol 60:167–181
Fernández C, Goldberg JM, Baird RA (1990) The vestibular nerve of the chinchilla. III. Peripheral innervation patterns in the utricular macula. J Neurophysiol 63:767–780
Fernández C, Lysakowski A, Goldberg JM (1995) Hair cell counts and afferent innervation patterns in the cristae ampullares of the squirrel monkey with a comparison to the chinchilla. J Neurophysiol 73:1253–1269
Fex J (1959) Augmentation of cochlear microphonic by stimulation of efferent fibres to the cochlea; preliminary report. Acta Otolaryngol 50:540–541
Fex J (1962) Auditory activity in centrifugal and centripetal cochlear fibres in cat. Acta Physiol Scand Suppl 189:1–68
Flock Å, Lam DM (1974) Neurotransmitter synthesis in inner ear and lateral line sense organs. Nature 249:142–144
Flock Å, Russell IJ (1973) The post-synaptic action of efferent fibres in the lateral line organ of the burbot Lota lota. J Physiol 235:591–605
Flock Å, Russell IJ (1976) Inhibition by efferent nerve fibres: action on hair cells and afferent synaptic transmission in the lateral line canal organ of the burbot Lota lota. J Physiol 257:45–62
Flores A, Soto E, Vega R (2001) Nitric oxide in the afferent synaptic transmission of the axolotl vestibular system. Neuroscience 103:457–464
Fontaine B, Klarsfeld A, Hökfelt T, Changeux JP (1986) Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci Lett 71:59–65
Fritzsch B (1981) Efferent neurons to the labyrinth of Salamandra salamandra as revealed by retrograde transport of horseradish peroxidase. Neurosci Lett 26:191–196
Fritzsch B, Crapon De Caprona D (1984) The origin of centrifugal inner ear fibers of Gymnophions (amphibia). A horseradish peroxidase study. Neurosci Lett 45:131–136
Fritzsch B, Dubuc R, Ohta Y, Grillner S (1989) Efferents to the labyrinth of the river lamprey (Lampetra fluviatilis) as revealed with retrograde tracing techniques. Neurosci Lett 96:241–246
Fuchs PA, Murrow BW (1992a) Cholinergic inhibition of short (outer) hair cells of the chick’s cochlea. J Neurosci 12:800–809
Fuchs PA, Murrow BW (1992b) A novel cholinergic receptor mediates inhibition of chick cochlear hair cells. Proc R Soc Lond B Biol Sci 248:35–40
Fukuda K, Higashida H, Kubo T, Maeda A, Akiba I, Bujo H, Mishina M, Numa S (1988) Selective coupling with K+ currents of muscarinic acetylcholine receptor subtypes in NG108-15 cells. Nature 335:355–358
Gacek RR (1960) Efferent component of the vestibular nerve. In: Rasmussen GL, Windle WF (eds) Neural mechanisms of the auditory and vestibular systems. Charles C. Thomas, Springfield, pp 276–284
Gacek RR, Lyon M (1974) The localization of vestibular efferent neurons in the kitten with horseradish peroxidase. Acta Otolaryngol (Stockh) 77:92–101
Gacek RR, Rasmussen GL (1961) Fiber analysis of statoacoustic nerve of guinea pig, cat and monkey. Anat Rec 139:455–463
Galambos R (1956) Suppression of the auditory nerve activity by stimulation of efferent fibers to the cochlea. J Neurophysiol 19:424–437
Garthwaite J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27:2783–2802
Gleisner L, Henriksson NG (1964) Efferent and afferent activity pattern in the vestibular nerve of the frog. Acta Otolaryngol Suppl (Stockh) 192:90–103
Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130:277–297
Goldberg JM, Chatlani S (2009) Repetitive discharge in vestibular nerve afferents. Association for Research in Otolaryngology Midwinter Meeting Abstracts 32:1106
Goldberg JM, Fernández C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34:635–660
Goldberg JM, Fernández C (1975) Responses of peripheral vestibular neurons to angular and linear accelerations in the squirrel monkey. Acta Otolaryngol (Stockh) 80:101–110
Goldberg JM, Fernández C (1977) Conduction times and background discharge of vestibular afferents. Brain Res 122:545–550
Goldberg JM, Fernández C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43:986–1025
Goldberg JM, Fernández C, Smith CE (1982) Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents. Brain Res 252:156–160
Goldberg JM, Smith CE, Fernández C (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
Goldberg JM, Desmadryl G, Baird RA, Fernández C (1990a) The vestibular nerve of the chinchilla. V. Relation between afferent discharge properties and peripheral innervation patterns in the utricular macula. J Neurophysiol 63:791–804
Goldberg JM, Lysakowski A, Fernández C (1990b) Morphophysiological and ultrastructural studies in the mammalian cristae ampullares. Hear Res 49:89–102
Goldberg JM, Brichta AM, Wackym PW (2000) Efferent vestibular system: anatomy, physiology and neurochemistry. In: Anderson JH, Beitz AJ (eds) Neurochemistry of the vestibular system. CRC Press, Boca Raton, pp 61–94
Guth PS, Norris CH, Guth SL, Quine DB, Williams WH (1986) Cholinomimetics mimic efferent effects on semicircular canal afferent activity in the frog. Acta Otolaryngol 102:194–203
Guth PS, Perin P, Norris CH, Valli P (1998) The vestibular hair cells: post-transductional signal processing. Prog Neurobiol 54:193–247
Guth PS, Holt JC, Lioudyno M, McIntosh JM, Hendricson AW, Athas GB, Shipon S (2002) The pharmacology of the non–α9/α10 nicotinic receptor of hair cells: clues as to subunit composition. Association for Research in Otolaryngology Midwinter Meeting Abstracts 25:480
Haque A, Angelaki DE, Dickman JD (2004) Spatial tuning and dynamics of vestibular semicircular canal afferents in rhesus monkeys. Exp Brain Res 155:81–90
Hartmann R, Klinke R (1980) Efferent activity in the goldfish vestibular nerve and its influence on afferent activity. Pflügers Arch 388:123–128
Hernandez CC, Zaika O, Tolstykh GP, Shapiro MS (2008) Regulation of neural KCNQ channels: signalling pathways, structural motifs and functional implications. J Physiol 586:1811–1821
Hiel H, Elgoyhen AB, Drescher DG, Morley BJ (1996) Expression of nicotinic acetylcholine receptor mRNA in the adult rat peripheral vestibular system. Brain Res 738:347–352
Highstein SM (1991) The central nervous system efferent control of the organs of balance and equilibrium. Neurosci Res 12:13–30
Highstein SM, Baker R (1985) Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. J Neurophysiol 54:370–384
Highstein SM, Baker R (1986) Organization of the efferent vestibular nuclei and nerves in the toadfish, Opsanus tau. J Comp Neurol 243:309–325
Hilding D, Wersäll J (1962) Cholinesterase and its relation to the nerve endings in the inner ear. Acta Otolaryngol (Stockh) 55:205–217
Hillman DE (1969) Light and electron microscopical study of the relationships between the cerebellum and the vestibular organ of the frog. Exp Brain Res 9:1–15
Hoffman LF, Honrubia V (2002) Fiber diameter distributions in the chinchilla’s ampullary nerves. Hear Res 172:37–52
Holstein GR, Martinelli GP, Boyle R, Rabbitt RD, Highstein SM (2004a) Ultrastructural observations of efferent terminals in the crista ampullaris of the toadfish, Opsanus tau. Exp Brain Res 157:128–136
Holstein GR, Martinelli GP, Henderson SC, Friedrich VL Jr, Rabbitt RD, Highstein SM (2004b) Gamma-aminobutyric acid is present in a spatially discrete subpopulation of hair cells in the crista ampullaris of the toadfish, Opsanus tau. J Comp Neurol 471:1–10
Holstein GR, Rabbitt RD, Martinelli GP, Friedrich VL Jr, Boyle RD, Highstein SM (2004c) Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses. Proc Natl Acad Sci U S A 101:15766–15771
Holt JC (2008) The effect of efferent stimulation on an afferent’s response to sinusoidal indentation in the turtle posterior crista. Association for Research in Otolaryngology Midwinter Meeting Abstracts 31:1249
Holt JC, Lioudyno M, Athas G, Garcia MM, Perin P, Guth PS (2001) The effect of proteolytic enzymes on the alpha9-nicotinic receptor-mediated response in isolated frog vestibular hair cells. Hear Res 152:25–42
Holt JC, Lioudyno M, Guth PS (2003) A pharmacologically distinct nicotinic ACh receptor is found in a subset of frog semicircular canal hair cells. J Neurophysiol 90:525–553
Holt JC, Lysakowski A, Goldberg JM (2006) Mechanisms of efferent-mediated responses in the turtle posterior crista. J Neurosci 26:13180–13193
Holt JC, Chatlani S, Lysakowski A, Goldberg JM (2007) Quantal and nonquantal transmission in calyx-bearing fibers of the turtle posterior crista. J Neurophysiol 98:1083–1101
Holt JC, Klapczynski M, Price SD, McIntosh JM, Goldberg JM, Lysakowski A (2008) Efferent cholinergic receptors in the turtle posterior crista. Association for Research in Otolaryngology Midwinter Meeting Abstracts 31:1108
Holt JC, Jordan P, Shah A, Barsz K (2010) Efferent-mediated excitation of turtle calyx-bearing afferents does not involve α9/10nAChRs. Association for Research in Otolaryngology Midwinter Meeting Abstracts 33:543
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
Hurley KM, Gaboyard S, Zhong M, Price SD, Wooltorton JR, 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 26:10253–10269
Ireland PE, Farakashidy J (1961) Studies on the efferent innervation of the vestibular end-organs. Trans Am Otol Soc 49:20–30
Ishiyama A, López I, Wackym PA (1994) Subcellular innervation patterns of the calcitonin gene related peptidergic efferent terminals in the chinchilla vestibular periphery. Otolaryngol Head Neck Surg 111:385–395
Iurato S, Luciano L, Pannese E, Reale E (1972) Efferent vestibular fibers in mammals: morphological and histochemical aspects. Prog Brain Res 37:429–443
Jordan P, Shah A, Barsz K, Holt JC (2010) Activation of muscarinic ACh receptors underlies efferent-mediated slow excitation in calyx-bearing afferents of the turtle posterior semicircular canal. Association for Research in Otolaryngology Midwinter Meeting Abstracts 33:555
Keller EL (1976) Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 24:459–471
Kharkovets T, Hardelin J-P, Safieddine S, Schweizer M, El-Amraoui A, Petit C, Jentsch TJ (2000) KCNQ4, a K+ channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc Nat Acad Sci U S A 97:4333–4338
Klinke R, Schmidt CL (1968) Efferente Impulse in Nervus vestibularis bei Reizung des kontralateralen Otolithenorgans. Pflügers Arch 304:183–188
Klinke R, Schmidt C (1970) Efferent influence on the vestibular organ during active movement of the body. Pflügers Arch 318:325–332
Kong WJ, Egg G, Hussl B, Spoendlin H, Schrott-Fischer A (1994) Localization of CHaT-like immunoreactivity in the vestibular endorgans of the rat. Hear Res 75:191–200
Kong WJ, Hussl B, Thumfart WF, Schrott-Fischer A (1998) Ultrastructural localization of GABA-like immunoreactivity in the vestibular periphery of the rat. Acta Otolaryngol 118:90–95
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
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
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
Li GQ, Kevetter GA, Leonard RB, Prusak DJ, Wood TG, Correia MJ (2007) Muscarinic acetylcholine receptor subtype expression in avian vestibular hair cells, nerve terminals and ganglion cells. Neuroscience 146:384–402
Lincoln J, Hoyle CHV, Burnstock G (1997) Nitric oxide in health and disease. Cambridge University Press, Cambridge
Lindeman HH (1969) Studies on the morphology of the sensory regions of the vestibular apparatus. Ergeb Anat Entwicklungsgesch 42:1–113
Lioudyno MI, Verbitsky M, Glowatzki E, Holt JC, Boulter J, Zadina JE, Elgoyhen AB, Guth PS (2002) The alpha9/alpha10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear. Mol Cell Neurosci 20:695–711
Lioudyno M, Hiel H, Kong JH, Katz E, Waldman E, Parameshwaran-Iyer S, Glowatzki E, Fuchs PA (2004) A “synaptoplasmic cistern” mediates rapid inhibition of cochlear hair cells. J Neurosci 24:11160–11164
Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346–354
Llinás R, Precht W (1969) The inhibitory vestibular efferent system and its relation to the cerebellum in the frog. Exp Brain Res 9:16–29
López I, Juiz JM, Altschuler RA, Meza G (1990) Distribution of GABA-like immunoreactivity in guinea pig vestibular cristae ampullaris. Brain Res 530:170–175
López I, Wu JY, Meza G (1992) Immunocytochemical evidence for an afferent GABAergic neurotransmission in the guinea pig vestibular system. Brain Res 589:341–348
Louie AW, Kimm J (1976) The response of 8th nerve fibers to horizontal sinusoidal oscillation in the alert monkey. Exp Brain Res 24:447–457
Luebke AE, Maroni PD, Guth SM, Lysakowski A (2005) Alpha-9 nicotinic acetylcholine receptor immunoreactivity in the rodent vestibular labyrinth. J Comp Neurol 492:323–333
Lustig LR, Hiel H, Fuchs PA (1999) Vestibular hair cells of the chick express the nicotinic acetylcholine receptor subunit alpha 9. J Vestib Res 9:359–367
Lysakowski A (1996) Synaptic organization of the crista ampullaris in vertebrates. Ann N Y Acad Sci 781:164–182
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
Lysakowski A, Goldberg JM (2004) Morphophysiology of the vestibular periphery. In: Highstein SM, Popper A, Fay RR (eds) The vestibular system. Springer, New York, pp 57–152
Lysakowski A, Goldberg JM (2008) Ultrastructural analysis of the cristae ampullares in the squirrel monkey (Saimiri sciureus). J Comp Neurol 511:47–64
Lysakowski A, Singer M (2000) Nitric oxide synthase localized in a subpopulation of vestibular efferents with NADPH diaphorase histochemistry and nitric oxide synthase immunohistochemistry. J Comp Neurol 427:508–521
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
Lysakowski A, Alonto A, Jacobson L (1999) Peripherin immunoreactivity labels small diameter vestibular “bouton” afferents in rodents. Hear Res 133:149–154
Marco J, Lee W, Suarez C, Hoffman L, Honrubia V (1993) Morphologic and quantitative study of the efferent vestibular system in the chinchilla: 3-D reconstruction. Acta Otolaryngol (Stockh) 113:229–234
Marlinski V, Plotnik M, Goldberg JM (2004) Efferent actions in the chinchilla vestibular labyrinth. J Assoc Res Otolaryngol 5:126–143
Marlinsky VV (1995) The effect of somatosensory stimulation on second-order and efferent vestibular neurons in the decerebrate decerebellate guinea-pig. Neuroscience 69:661–669
Matsubara A, Usami S, Fujita S, Shinkawa H (1995) Expression of substance P, CGRP, and GABA in the vestibular periphery, with special reference to species differences. Acta Otolaryngol Suppl 519:248–252
Matsuda Y (1996) Localization of choline acetyltransferase and calcitonin gene-related peptide immunoreactivities in the vestibular end-organs of the guinea pig. Osaka City Med J 42:61–76
McCue MP, Guinan JJ Jr (1994) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J Neurosci 14:6071–6083
Meredith GE (1988) Comparative view of the central organization of afferent and efferent circuitry for the inner ear. Acta Biol Hung 39:229–249
Meredith GE, Roberts BL (1987) Distribution and morphological characteristics of efferent neurons innervating end organs in the ear and lateral line of the european eel. J Comp Neurol 265:494–506
Millar NS, Gotti C (2009) Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56:237–246
Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109–142
Narins PM, Lewis ER (1984) The vertebrate ear as an exquisite seismic sensor. J Acoust Soc Am 76:1384–1387
New HV, Mudge AW (1986) Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809–811
Nomura Y, Gacek RR, Balogh KJ (1965) Efferent innervation of vestibular labyrinth. Arch Otolaryngol 81:335–339
Ohno K, Takeda N, Yamano M, Matsunaga T, Tohyama M (1991) Coexistence of acetylcholine and calcitonin gene-related peptide in the vestibular efferent neurons in the rat. Brain Res 566:103–107
Ohno K, Takeda N, Kiyama H, Kato H, Fujita S, Matsunaga T, Tohyama M (1993) Synaptic contact between vestibular afferent nerve and cholinergic efferent terminal: its putative mediation by nicotinic receptors. Brain Res Mol Brain Res 18:343–346
Oliver D, Klocker N, Schuck J, Baukrowitz T, Ruppersberg JP, Fakler B (2000) Gating of Ca2+-activated K+ channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron 26:595–601
Palay SL, Palade GE (1955) The fine structure of neurons. J Biophys Biochem Cytol 1:69–88
Pellergrini M, Ceccotti F, Magherini P (1985) The efferent vestibular neurons in the toad (Bufo bufo L.): their location and morphology. A horseradish peroxidase study. Brain Res 344:1–8
Perachio AA, Correia MJ (1983) Responses of semicircular canal and otolith afferents to small angle static head tilts in the gerbil. Brain Res 280:287–298
Perachio AA, Kevetter GA (1989) Identification of vestibular efferent neurons in the gerbil: histochemical and retrograde labelling. Exp Brain Res 78:315–332
Pérez C, Limón A, Vega R, Soto E (2009a) 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
Pérez C, Vega R, Soto E (2009b) Phospholipase C-mediated inhibition of the M-potassium current by muscarinic-receptor activation in the vestibular primary-afferent neurons of the rat. Neurosci Lett 468:238–242
Plotnik M, Marlinski V, Goldberg JM (2002) Reflections of efferent activity in rotational responses of chinchilla vestibular afferents. J Neurophysiol 88:1234–1244
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
Popper P, Wackym PA (2001) Opioid peptides and receptors in the vestibular epithelia in rats. In: 31st SFN meeting, abstract 298.28
Popper P, Cristobal R, Wackym PA (2004) Expression and distribution of mu opioid receptors in the inner ear of the rat. Neuroscience 129:225–233
Precht W, Llinás R, Clarke M (1971) Physiological responses of frog vestibular fibers to horizontal angular rotation. Exp Brain Res 13:378–407
Prigioni I, Valli P, Casella C (1983) Peripheral organization of the vestibular efferent system in the frog: an electrophysiological study. Brain Res 269:83–90
Purcell IM, Perachio AA (1997) Three-dimensional analysis of vestibular efferent neurons innervating semicircular canals of the gerbil. J Neurophysiol 78:3234–3248
Rasmussen GL (1946) The olivary peduncle and other fiber connections of the superior olivary complex. J Comp Neurol 84:141–219
Rasmussen GL (1953) Further observations of the efferent cochlear bundle. J Comp Neurol 99:61–74
Rasmussen GL, Gacek RR (1958) Concerning the question of the efferent fiber component of the vestibular nerve of the cat. Anat Rec 130:361–362
Rennie KJ (2002) Modulation of the resting potassium current in type I vestibular hair cells by cGMP. In: Berlin CI, Hood LJ, Ricci AJ (eds) Hair cell micromechanics and otoacoustic emissions. Singular Press, Clifton Park, pp 79–89
Rennie KJ, Ashmore JF (1993) Effects of extracellular ATP on hair cells isolated from the guinea-pig semicircular canals. Neurosci Lett 160:185–189
Roberts BL, Russell IJ (1972) The activity of lateral line efferent neurones in stationary and swimming dogfish. J Exp Biol 57:433–448
Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304:129–135
Rossi G, Cortesina G (1965) The “efferent cochlear and vestibular system” in Lepus cuniculus L. Acta Anat 60:362–381
Rossi ML, Martini M (1991) Efferent control of posterior canal afferent receptor discharge in the frog labyrinth. Brain Res 555:123–134
Rossi ML, Prigioni I, Valli P, Casella C (1980) Activation of the efferent system in the isolated frog labyrinth: effects on the afferent EPSPs and spike discharge recorded from single fibres of the posterior nerve. Brain Res 185:125–137
Rossi ML, Martini M, Pelucchi B, Fesce R (1994) Quantal nature of synaptic transmission at the cytoneural junction in the frog labyrinth. J Physiol (Lond) 478:17–35
Russell IJ (1968) Influence of efferent fibres on a receptor. Nature 219:177–178
Russell IJ (1971) The role of the lateral-line efferent system in Xenopus laevis. J Exp Biol 54:621–641
Ryan AF, Simmons DM, Watts AG, Swanson LW (1991) Enkephalin mRNA production by cochlear and vestibular efferent neurons in the gerbil brainstem. Exp Brain Res 87:259–267
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
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
Sala O (1965) The efferent vestibular system. Electrophysiological research. Acta Otolaryngol Suppl 197:1–34
Sans A, Highstein SM (1984) New ultrastructural features in the vestibular labyrinth of the toadfish, Opsanus tau. Brain Res 306:191–195
Schmidt RS (1963) Frog labyrinthine efferent impulses. Acta Otolaryngol (Stockh) 56:51–64
Schneider LW, Anderson DJ (1976) Transfer characteristics of first and second order lateral canal vestibular neurons in gerbil. Brain Res 112:61–76
Schuknecht HF, Churchill JA, Doran R (1959) The localization of acetylcholine-esterase in the cochlea. AMA Arch Otolaryngol 69:549–559
Schwarz DWF, Satoh K, Schwarz IE, Hu K, Fibiger HC (1986) Cholinergic innervation of the rat’s labrinth. Exp Brain Res 64:19–26
Schweitzer E (1987) Coordinated release of ATP and ACh from cholinergic synaptosomes and its inhibition by calmodulin antagonists. J Neurosci 7:2948–2956
Selyanko AA, Hadley JK, Wood IC, Abogadie FC, Jentsch TJ, Brown DA (2000) Inhibition of KCNQ1-4 potassium channels expressed in mammalian cells via M1 muscarinic acetylcholine receptors. J Physiol (Lond) 522(Pt 3):349–355
Sewell WF, Starr PA (1991) Effects of calcitonin gene-related peptide and efferent nerve stimulation on afferent transmission in the lateral line organ. J Neurophysiol 65:1158–1169
Shah A, Barsz K, Jordan P, Parker D, Holt JC (2010) Efferent actions differentially affect afferent sensitivity to sinusoidal indentation in the turtle posterior semicircular canal. Association for Research in Otolaryngology Midwinter Meeting Abstracts 33:516
Shinder ME, Purcell IM, Kaufman GD, Perachio AA (2001) Vestibular efferent neurons project to the flocculus. Brain Res 889:288–294
Silinsky EM (1975) On the association between transmitter secretion and the release of adenine nucleotides from mammalian motor nerve terminals. J Physiol 247:145–162
Smith CE, Goldberg JM (1986) A stochastic afterhyperpolarization model of repetitive activity in vestibular afferents. Biol Cybern 54:41–51
Smith CA, Rasmussen GL (1968) Nerve ending in the maculae and cristae of the chinchilla vestibule, with a special reference to the efferents. In: Graybiel A (ed) The third symposium on the role of the vestibular organs in space exploration. U.S. Government Printing Office, Washington, pp 183–201
Sousa AD, Andrade LR, Salles FT, Pillai AM, Buttermore ED, Bhat MA, Kachar B (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
Sridhar TS, Liberman MC, Brown MC, Sewell WF (1995) A novel cholinergic “slow effect” of efferent stimulation on cochlear potentials in the guinea pig. J Neurosci 15:3667–3678
Sridhar TS, Brown MC, Sewell WF (1997) Unique postsynaptic signaling at the hair cell efferent synapse permits calcium to evoke changes on two time scales. J Neurosci 17:428–437
Stocker M (2004) Ca2+-activated K+ channels: molecular determinants and function of the SK family. Nat Rev Neurosci 5:758–770
Strutz J (1981) The origin of centrifugal fibers to the inner ear in Caiman crocodilus. A HRP study. Neurosci Lett 27:65–100
Strutz J (1982a) The origin of efferent fibers to the inner ear in a turtle (Terrapene ornata). A horseradish peroxidase study. Brain Res 244:165–168
Strutz J (1982b) The origin of efferent vestibular fibers in the guinea pig. Acta Otolaryngol (Stockh) 94:299–305
Strutz J, Schmidt CL (1982) Acoustic and vestibular efferent neurons in the chicken (Gallus domesticus). Acta Otolaryngol (Stockh) 94:45–51
Sugai T, Sugitani M, Ooyama H (1991) Effects of activation of the divergent efferent fibers on the spontaneous activity of vestibular afferent fibers in the toad. Jpn J Physiol 41:217–232
Syeda SN, Lysakowski A (2001) P2X2 purinergic receptor localized in the inner ear. Association for Research in Otolaryngology Midwinter Meeting Abstracts 24:19
Takumida M, Anniko M (2002) Nitric oxide in the inner ear. Curr Opin Neurol 15:11–15
Taly A, Corringer PJ, Guedin D, Lestage P, Changeux JP (2009) Nicotinic receptors: allosteric transitions and therapeutic targets in the nervous system. Nat Rev Drug Discov 8:733–750
Tanaka M, Takeda N, Senba E, Tohyama M, Kubo T, Matsunaga T (1989) Localization, origin and fine structure of calcitonin gene related peptide-containing fibers in the vestibular end-organs of the rat. Brain Res 504:31–35
Tomko DL, Peterka RJ, Schor RH, O’Leary DP (1981) Response dynamics of horizontal canal afferents in barbiturate-anesthetized cats. J Neurophysiol 45:376–396
Troyanovskaya M, Wackym PA (1998) Evidence for three additional P2X2 purinoceptor isoforms produced by alternative splicing in the adult rat vestibular end-organs. Hear Res 126:201–209
Usami S-I, Igarashi M, Thompson G (1987) GABA-like immunoreactivity in the squirrel monkey vestibular endorgans. Brain Res 417:367–370
Usami S, Hozawa J, Tazawa M, Igarashi M, Thompson GC, Wu JY, Wenthold RJ (1989) Immunocytochemical study of the GABA system in chicken vestibular endorgans and the vestibular ganglion. Brain Res 503:214–218
Vega R, Soto E (2003) Opioid receptors mediate a postsynaptic facilitation and a presynaptic inhibition at the afferent synapse of axolotl vestibular hair cells. Neuroscience 118:75–85
Wackym PA, Popper P, Ward PH, Micevych PE (1991) Cell and molecular anatomy of nicotinic acetylcholine receptor subunits and calcitonin gene-related peptide in the rat vestibular system. Otolaryngol Head Neck Surg 105:493–510
Wackym PA, Popper P, López I, Ishiyama A, Micevych PE (1995) Expression of alpha 4 and beta 2 nicotinic acetylcholine receptor subunit mRNA and localization of alpha-bungarotoxin binding proteins in the rat vestibular periphery. Cell Biol Int 19:291–300
Wackym PA, Chen CT, Ishiyama A, Pettis RM, López IA, Hoffman L (1996) Muscarinic acetylcholine receptor subtype mRNAs in the human and rat vestibular periphery. Cell Biol Int 20:187–192
Walsh EJ, McGee J, McFadden SL, Liberman MC (1998) Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J Neurosci 18:3859–3869
Warr WB (1975) Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol 161:159–182
Weisstaub N, Vetter DE, Elgoyhen AB, Katz E (2002) The alpha9alpha10 nicotinic acetylcholine receptor is permeable to and is modulated by divalent cations. Hear Res 167:122–135
Wersäll J, Bagger-Sjöbäck D (1974) Morphology of the vestibular sense organ. In: Kornhuber HH (ed) Handbook of sensory physiology, vol. VI. Vestibular system. Part 1. Basic mechanisms. Springer, Berlin, pp 123–170
White JS (1985) Fine structure of vestibular efferent neurons in the albino rat. Soc Neurosci Abstr 11:322
Whitehead MC, Morest DK (1981) Dual populations of efferent and afferent cochlear axons in the chicken. Neuroscience 6:2351–2365
Wilson VJ, Melvill Jones G (1979) Mammalian vestibular physiology. Plenum Press, New York
Wong LA, Gallagher JP (1991) Pharmacology of nicotinic receptor-mediated inhibition in rat dorsolateral septal neurones. J Physiol 436:325–346
Yagi T, Simpson NE, Markham CH (1977) The relationship of conduction velocity to other physiological properties of the cat’s horizontal canal neurons. Exp Brain Res 30:587–600
Yamaguchi K, Ohmori H (1993) Suppression of the slow K+ current by cholinergic agonists in cultured chick cochlear ganglion neurones. J Physiol (Lond) 464:213–228
Yoshida N, Shigemoto T, Sugai T, Ohmori H (1994) The role of inositol trisphosphate on ACh-induced outward currents in bullfrog saccular hair cells. Brain Res 644:90–100
Yuhas WA, Fuchs PA (1999) Apamin-sensitive, small-conductance, calcium-activated potassium channels mediate cholinergic inhibition of chick auditory hair cells. J Comp Physiol A 185:455–462
Zheng XY, Henderson D, McFadden SL, Ding DL, Salvi RJ (1999) Auditory nerve fiber responses following chronic cochlear de-efferentation. J Comp Neurol 406:72–86
Acknowledgments
Research in the authors’ laboratories is supported by Grants NIDCD DC08981 (JCH), NIDCD DC02521 (AL), and NIDCD DC02508 (JMG). The authors also thank Erika Bruss for providing the animal illustrations used in several of the figures.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Holt, J.C., Lysakowski, A., Goldberg, J.M. (2011). The Efferent Vestibular System. In: Ryugo, D., Fay, R. (eds) Auditory and Vestibular Efferents. Springer Handbook of Auditory Research, vol 38. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7070-1_6
Download citation
DOI: https://doi.org/10.1007/978-1-4419-7070-1_6
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4419-7069-5
Online ISBN: 978-1-4419-7070-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)