Skip to main content
SpringerLink
Log in

Development of the Inner Ear Efferent System

  • Chapter
  • First Online:
Auditory and Vestibular Efferents

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 38))

Abstract

Roberts and Meredith (1992) wrote: “For more than forty years, the efferent supply to the mammalian ear provided by the olivocochlea bundle has been an enigma,” and this is still true today, in particular for the development of efferents. The inner ear efferents are so unique in their physiology, axonal course, and distribution that this adds to the mystery of their role in hearing and balance (Christopher Kirk and Smith 2003). However, analyzing the development of the vestibulocochlear efferent system may not only give us new insight into the development of this system but may also help to understand how the distribution and neurochemcial properties of the adult vestibulocochlear efferent system all come about.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adams JC (1983) Cytology of periolivary cells and the organization of their projections in the cat. J Comp Neurol 215:275–289

    Article  CAS  PubMed  Google Scholar 

  • Altman J, Bayer SA (1982) Development of the cranial nerve ganglia and related nuclei in the rat. Adv Anat Embryol Cell Biol 74:1–90

    Article  CAS  PubMed  Google Scholar 

  • Altschuler RA, Fex J, Parakkal MH, Eckenstein F (1984) Co-localization of enkephalin-like and choline acetyltransferase-like immunoreactivities in olivocochlear neurons of the guinea pig. J Histochem Cytochem 32:839–843

    Article  CAS  PubMed  Google Scholar 

  • Apel ED, Glass DJ, Moscoso LM, Yancopoulos GD, Sanes JR (1997) Rapsyn is required for MuSK signaling and recruits synaptic components to a MuSK-containing scaffold. Neuron 18:623–635

    Article  CAS  PubMed  Google Scholar 

  • Bergeron AL, Schrader A, Yang D, Osman AA, Simmons DD (2005) The final stage of cholinergic differentiation occurs below inner hair cells during development of the rodent cochlea. J Assoc Res Otolaryngol 6:401–415

    Article  PubMed  PubMed Central  Google Scholar 

  • Briscoe J, Ericson J (2001) Specification of neuronal fates in the ventral neural tube. Curr Opin Neurobiol 11:43–49

    Article  CAS  PubMed  Google Scholar 

  • Brown MC (1987) Morphology of labeled efferent fibers in the guinea pig cochlea. J Comp Neurol 260:605–618

    Article  CAS  PubMed  Google Scholar 

  • Bruce LL, Kingsley J, Nichols DH, Fritzsch B (1997) The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15:671–692

    Article  CAS  PubMed  Google Scholar 

  • Bruce LL, Christensen MA, Warr WB (2000) Postnatal development of efferent synapses in the rat cochlea. J Comp Neurol 423:532–548

    Article  CAS  PubMed  Google Scholar 

  • Canlon B, Cartaud J, Changeux JP (1989) Localization of alpha-bungarotoxin binding sites on outer hair cells from the guinea-pig cochlea. Acta Physiol Scand 137:549–550

    Article  CAS  PubMed  Google Scholar 

  • Cheng A, Bollan KA, Greenwood SM, Irving AJ, Connolly CN (2007) Differential subcellular localization of RIC-3 isoforms and their role in determining 5-HT3 receptor composition. J Biol Chem 282:26158–26166

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Christopher Kirk E, Smith DW (2003) Protection from acoustic trauma is not a primary function of the medial olivocochlear efferent system. J Assoc Res Otolaryngol 4:445–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole KS, Robertson D (1992) Early efferent innervation of the developing rat cochlea studied with a carbocyanine dye. Brain Res 575:223–230

    Article  CAS  PubMed  Google Scholar 

  • Cowan CA, Yokoyama N, Bianchi LM, Henkemeyer M, Fritzsch B (2000) EphB2 guides axons at the midline and is necessary for normal vestibular function. Neuron 26:417–430

    Article  CAS  PubMed  Google Scholar 

  • Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KS, Pevny LH, Kelley MW (2008) Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc Natl Acad Sci USA 105:18396–18401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dememes D, Dechesne CJ, Venteo S, Gaven F, Raymond J (2001) Development of the rat efferent vestibular system on the ground and in microgravity. Brain Res Dev Brain Res 128:35–44

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dulon D, Lenoir M (1996) Cholinergic responses in developing outer hair cells of the rat cochlea. Eur J Neurosci 8:1945–1952

    Article  CAS  PubMed  Google Scholar 

  • 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 USA 98:3501–3506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eybalin M (1993) Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73:309–373

    Article  CAS  PubMed  Google Scholar 

  • Eybalin M, Pujol R (1984) Immunofluorescence with Met-enkephalin and Leu-enkephalin antibodies in the guinea pig cochlea. Hear Res 13:135–140

    Article  CAS  PubMed  Google Scholar 

  • Favre D, Sans A (1977) Synaptogenesis of the efferent vestibular nerve endings of the cat: ultrastructural study. Arch Otorhinolaryngol 215:183–186

    Article  CAS  PubMed  Google Scholar 

  • Felix D, Ehrenberger K (1992) The efferent modulation of mammalian inner hair cell afferents. Hear Res 64:1–5

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B (1992) The water-to-land transition: evolution of the tetrapod basilar papilla, middle ear and auditory nuclei. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 351–375

    Chapter  Google Scholar 

  • Fritzsch B (1999) Ontogenetic and evolutionary evidence for the motoneuron nature of vestibular and cochlear efferents. In: Berlin C (ed) The efferent auditory system: basic science and clinical applications. Singular Publishing, San Diego, p 31

    Google Scholar 

  • Fritzsch B, Nichols DH (1993) DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. Hear Res 65:51–60

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Northcutt RG (1993) Origin and migration of trochlear, oculomotor and abducent motor neurons in Petromyzon marinus L. Brain Res Dev Brain Res 74:122–126

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Christensen MA, Nichols DH (1993) Fiber pathways and positional changes in efferent perikarya of 2.5- to 7-day chick embryos as revealed with DiI and dextran amines. J Neurobiol 24:1481–1499

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Pirvola U, Ylikoski J (1999) Making and breaking the innervation of the ear: neurotrophic support during ear development and its clinical implications. Cell Tissue Res 295:369–382

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Muirhead KA, Feng F, Gray BD, Ohlsson-Wilhelm BM (2005) Diffusion and imaging properties of three new lipophilic tracers, NeuroVue Maroon, NeuroVue Red and NeuroVue Green and their use for double and triple labeling of neuronal profile. Brain Res Bull 66:249–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritzsch B, Pauley S, Beisel KW (2006) Cells, molecules and morphogenesis: the making of the vertebrate ear. Brain Res 1091:151–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gacek RR, Nomura Y, Balogh K (1965) Acetylcholinesterase activity in the efferent fibers of the stato-acoustic nerve. Acto Otolaryngol 59:541–553

    Article  CAS  Google Scholar 

  • Gaufo GO, Flodby P, Capecchi MR (2000) Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development (Cambridge, UK) 127:5343–5354

    Article  CAS  Google Scholar 

  • Ginzberg RD, Morest DK (1984) Fine structure of cochlear innervation in the cat. Hear Res 14:109–127

    Article  CAS  PubMed  Google Scholar 

  • Glowatzki E, Fuchs PA (2000) Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 288:2366–2368

    Article  CAS  PubMed  Google Scholar 

  • Goldberg JM, Lysakowski A, Fernandez C (1992) Structure and function of vestibular nerve fibers in the chinchilla and squirrel monkey. Ann NY Acad Sci 656:92–107

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Casati ME, Fuchs PA, Elgoyhen AB, Katz E (2005) Biophysical and pharmacological characterization of nicotinic cholinergic receptors in rat cochlear inner hair cells. J Physiol 566:103–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, Kolodkin AL, Ginty DD (2003) Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 5:45–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gurung B, Fritzsch B (2004) Time course of embryonic midbrain thalamic and thalamic auditory connection development in mice as revealed by carbocyannine dye injection. J Comp Neurol 479:309–327

    Article  PubMed  PubMed Central  Google Scholar 

  • He DZ, Dallos P (1999) Development of acetylcholine-induced responses in neonatal gerbil outer hair cells. J Neurophysiol 81:1162–1170

    Article  CAS  PubMed  Google Scholar 

  • He DZ, Evans BN, Dallos P (1994) First appearance and development of electromotility in neonatal gerbil outer hair cells. Hear Res 78:77–90

    Article  CAS  PubMed  Google Scholar 

  • He DZ, Zheng J, Dallos P (2001) Development of acetylcholine receptors in cultured outer hair cells. Hear Res 162:113–125

    Article  CAS  PubMed  Google Scholar 

  • Iurato S, Smith CA, Eldredge DH, Henderson D, Carr C, Ueno Y, Cameron S, Richter R (1978) Distribution of the crossed olivocochlear bundle in the chinchilla’s cochlea. J Comp Neurol 182:57–76

    Article  CAS  PubMed  Google Scholar 

  • Jagger DJ, Griesinger CB, Rivolta MN, Holley MC, Ashmore JF (2000) Calcium signalling mediated by the alpa 9 acetylcholine receptor in a cochlear cell line from the Immortomouse. J Physiol 527:49–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins SA, Simmons DD (2006) GABAergic neurons in the lateral superior olive of the hamster are distinguished by differential expression of GAD isoforms during development. Brain Res 1111:12–25

    Article  CAS  PubMed  Google Scholar 

  • Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, de Caprona D, Fritzsch B (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429:615–630

    Article  CAS  PubMed  Google Scholar 

  • Katz E, Elgoyhen AB, Gomez-Casati ME, Knipper M, Vetter DE, Fuchs PA, Glowatzki E (2004) Developmental regulation of nicotinic synapses on cochlear inner hair cells. J Neurosci 24:7814–7820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim WY, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, Lee JE (2001) NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128:417–426

    Article  CAS  PubMed  Google Scholar 

  • Klocker N, Oliver D, Ruppersberg JP, Knaus HG, Fakler B (2001) Developmental expression of the small-conductance Ca(2+)-activated potassium channel SK2 in the rat retina. Mol Cell Neurosci 17:514–520

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol 301:443–460

    Article  CAS  PubMed  Google Scholar 

  • Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee KF (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410:1057–1064

    Article  CAS  PubMed  Google Scholar 

  • Lopez I, Meza G (1990) Comparative studies on glutamate decarboxylase and choline acetyltransferase activities in the vertebrate vestibule. Comp Biochem Physiol B 95:375–379

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Bennett T, Jung HH, Ryan AF (1998) Developmental expression of alpha 9 acetylcholine receptor mRNA in the rat cochlea and vestibular inner ear. J Comp Neurol 393:320–331

    Article  CAS  PubMed  Google Scholar 

  • Lysakowski A, Goldberg JM (2008) Ultrastructural analysis of the cristae ampullares in the squirrel monkey (Saimiri sciureus). J Comp Neurol 511:47–64

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma Q, Sommer L, Cserjesi P, Anderson DJ (1997) Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J Neurosci 17:3644–3652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Q, Anderson DJ, Fritzsch B (2000) Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J Assoc Res Otolaryngol JARO 1:129–143

    Article  CAS  PubMed  Google Scholar 

  • Maison SF, Adams JC, Liberman MC (2003a) Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J Comp Neurol 455:406–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maison SF, Emeson RB, Adams JC, Luebke AE, Liberman MC (2003b) Loss of alpha CGRP reduces sound-evoked activity in the cochlear nerve. J Neurophysiol 90:2941–2949

    Article  CAS  PubMed  Google Scholar 

  • Maison SF, Rosahl TW, Homanics GE, Liberman MC (2006) Functional role of GABAergic innervation of the cochlea: phenotypic analysis of mice lacking GABA(A) receptor subunits alpha 1, alpha 2, alpha 5, alpha 6, beta 2, beta 3, or delta. J Neurosci 26:10315–10326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maklad A, Fritzsch B (1999) Incomplete segregation of endorgan-specific vestibular ganglion cells in mice and rats. J Vestib Res 9:387–399

    Article  CAS  PubMed  Google Scholar 

  • Maklad A, Fritzsch B (2003) Development of vestibular afferent projections into the hindbrain and their central targets. Brain Res Bull 60:497–510

    Article  PubMed  PubMed Central  Google Scholar 

  • Mbiene JP, Favre D, Sans A (1988) Early innervation and differentiation of hair cells in the vestibular epithelia of mouse embryos: SEM and TEM study. Anat Embryol (Berl) 177:331–340

    Article  CAS  Google Scholar 

  • Merchan-Perez A, Bartolome MV, Ibanez MA, Gil-Loyzaga P (1993) Expression of GAP-43 in growing efferent fibers during cochlear development. ORL J Otorhinolaryngol Relat Spec 55:208–210

    Article  CAS  PubMed  Google Scholar 

  • Merchan-Perez A, Gil-Loyzaga P, Eybalin M, Fernandez Mateos P, Bartolome MV (1994) Choline-acetyltransferase-like immunoreactivity in the organ of Corti of the rat during postnatal development. Brain Res Dev Brain Res 82:29–34

    Article  CAS  PubMed  Google Scholar 

  • Meza G (2008) Modalities of GABA and glutamate neurotransmission in the vertebrate inner ear vestibule. Neurochem Res 33:1634–1642

    Article  CAS  PubMed  Google Scholar 

  • Moore JK, Simmons DD, Guan Y (1999) The human olivocochlear system: organization and development. Audiol Neurootol 4:311–325

    Article  CAS  PubMed  Google Scholar 

  • Morley BJ, Simmons DD (2002) Developmental mRNA expression of the alpha10 nicotinic acetylcholine receptor subunit in the rat cochlea. Brain Res Dev Brain Res 139:87–96

    Article  CAS  PubMed  Google Scholar 

  • Morris JK, Maklad A, Hansen LA, Feng F, Sorensen C, Lee KF, Macklin WB, Fritzsch B (2006) A disorganized innervation of the inner ear persists in the absence of ErbB2. Brain Res 1091:186–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller M, Jabs N, Lorke DE, Fritzsch B, Sander M (2003) Nkx6.1 controls migration and axon pathfinding of cranial branchio-motoneurons. Development (Cambridge, UK) 130: 5815–5826

    Article  CAS  Google Scholar 

  • Murthy V, Maison SF, Taranda J, Haque N, Bond CT, Elgoyhen AB, Adelman JP, Liberman MC, Vetter DE (2009) SK2 channels are required for function and long-term survival of efferent synapses on mammalian outer hair cells. Mol Cell Neurosci 40:39–49

    Article  CAS  PubMed  Google Scholar 

  • Nichols DH, Pauley S, Jahan I, Beisel KW, Millen KJ, Fritzsch B (2008) Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. Cell Tissue Res 334:339–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitecka LM, Sobkowicz HM (1996) The GABA/GAD innervation within the inner spiral bundle in the mouse cochlea. Hear Res 99:91–105

    Article  CAS  PubMed  Google Scholar 

  • Nordemar H (1983) Embryogenesis of the inner ear. II. The late differentiation of the mammalian crista ampullaris in vivo and in vitro. Acta Otolaryngol 96:1–8

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ohsawa R, Ohtsuka T, Kageyama R (2005) Mash1 and Math3 are required for development of branchiomotor neurons and maintenance of neural progenitors. J Neurosci 25:5857–5865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osen KK, Mugnaini E, Dahl AL, Christiansen AH (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. Arch Ital Biol 122:169–212

    CAS  PubMed  Google Scholar 

  • Osman AA, Schrader AD, Hawkes AJ, Akil O, Bergeron A, Lustig LR, Simmons DD (2008) Muscle-like nicotinic receptor accessory molecules in sensory hair cells of the inner ear. Mol Cell Neurosci 38:153–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattyn A, Hirsch M, Goridis C, Brunet JF (2000) Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development (Cambridge, UK) 127:1349–1358

    Article  CAS  Google Scholar 

  • Perachio AA, Kevetter GA (1989) Identification of vestibular efferent neurons in the gerbil: histochemical and retrograde labelling. Exp Brain Res 78:315–326

    Article  CAS  PubMed  Google Scholar 

  • Pirvola U, Ylikoski J, Palgi J, Lehtonen E, Arumae U, Saarma M (1992) Brain-derived neurotrophic factor and neurotrophin 3 mRNAs in the peripheral target fields of developing inner ear ganglia. Proc Natl Acad Sci USA 89:9915–9999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popper P, Ishiyama A, Lopez I, Wackym PA (2002) Calcitonin gene-related Peptide and choline acetyltransferase colocalization in the human vestibular periphery. Audiol Neurootol 7:298–302

    Article  CAS  PubMed  Google Scholar 

  • Puel JL, Ruel J, Guitton M, Wang J, Pujol R (2002) The inner hair cell synaptic complex: physiology, pharmacology and new therapeutic strategies. Audiol Neurootol 7:49–54

    Article  CAS  PubMed  Google Scholar 

  • Pujol R, Carlier E, Devigne C (1978) Different patterns of cochlear innervation during the development of the kitten. J Comp Neurol 177:529–536

    Article  CAS  PubMed  Google Scholar 

  • Puligilla C, Feng F, Ishikawa K, Bertuzzi S, Dabdoub A, Griffith AJ, Fritzsch B, Kelley MW (2007) Disruption of fibroblast growth factor receptor 3 signaling results in defects in cellular differentiation, neuronal patterning, and hearing impairment. Dev Dyn 236:1905–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purcell IM, Perachio AA (1997) Three-dimensional analysis of vestibular efferent neurons innervating semicircular canals of the gerbil. J Neurophysiol 78:3234–3248

    Article  CAS  PubMed  Google Scholar 

  • Raji-Kubba J, Micevych PE, Simmons DD (2002) Superior olivary complex of the hampster has multiple periods of cholinergic neuron development. J Chem Neuroanat 24:75–93

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1977) Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond B Biol Sci 278:245–260

    Article  CAS  PubMed  Google Scholar 

  • Reuss S, Disque-Kaiser U, Antoniou-Lipfert P, Gholi MN, Riemann E, Riemann R (2009) Neurochemistry of olivocochlear neurons in the hamster. Anat Rec 292:461–471

    Article  Google Scholar 

  • Roberts BL, Meredith GE (1992) The efferent innervation of the ear: variations on an enigma. In: Webster DB, Fay RR, Popper AN, editors. The Evolutionary Biology of Hearing. New York: Springer Verlag. pp. 185–210

    Chapter  Google Scholar 

  • Rohrschneider MR, Elsen GE, Prince VE (2007) Zebrafish Hoxb1a regulates multiple downstream genes including prickle1b. Dev Biol 309:358–372

    Article  CAS  PubMed  Google Scholar 

  • Rusch A, Lysakowski A, Eatock RA (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Safieddine S, Eybalin M (1992) Triple immunofluorescence evidence for the coexistence of acetylcholine, enkephalis, and calcitonin gene-related peptide within efferent neurons of rats and guinea pigs. Eur J Neurosci 4:981–992

    Article  PubMed  Google Scholar 

  • Schrott-Fischer A, Kammen-Jolly K, Scholtz A, Rask-Andersen H, Glueckert R, Eybalin M (2007) Efferent neurotransmitters in the human cochlea and vestibule. Acta Otolaryngol 127: 13–19

    Article  CAS  PubMed  Google Scholar 

  • Shatz CJ, Ghosh A, McConnell SK, Allendoerfer KL, Friauf E, Antonini A (1990) Pioneer neurons and target selection in cerebral cortical development. Cold Spring Harb Symp Quant Biol 55:469–480

    Article  CAS  PubMed  Google Scholar 

  • Simmons DD (2002) Development of the inner ear efferent system across vertebrate species. J Neurobiol 53:228–250

    Article  PubMed  Google Scholar 

  • Simmons DD, Morley BJ (1998) Differential expression of the alpha 9 nicotinic acetylcholine receptor subunit in neonatal and adult cochlear hair cells. Brain Res Mol Brain Res 56:287–292

    Article  CAS  PubMed  Google Scholar 

  • Simmons DD, Raji-Kubba J (1993) Postnatal calcitonin gene-related peptide in the superior olivary complex. J Chem Neuroanat 6:407–418

    Article  CAS  PubMed  Google Scholar 

  • Simmons DD, Manson-Gieseke L, Hendrix TW, McCarter S (1990) Reconstructions of efferent fibers in the postnatal hamster cochlea. Hear Res 49:127–139

    Article  CAS  PubMed  Google Scholar 

  • Simmons DD, Mansdorf NB, Kim JH (1996a) Olivocochlear innervation of inner and outer hair cells during postnatal maturation: evidence for a waiting period. J Comp Neurol 370:551–562

    Article  CAS  PubMed  Google Scholar 

  • Simmons DD, Moulding HD, Zee D (1996b) Olivocochlear innervation of inner and outer hair cells during postnatal maturation: an immunocytochemical study. Brain Res Dev Brain Res 95:213–226

    Article  CAS  PubMed  Google Scholar 

  • Simmons DD, Bertolotto C, Kim J, Raji-Kubba J, Mansdorf N (1998) Choline acetyltransferase expression during a putative developmental waiting period. J Comp Neurol 397:281–295

    Article  CAS  PubMed  Google Scholar 

  • Simon H, Lumsden A (1993) Rhombomere-specific origin of the contralateral vestibulo-acoustic efferent neurons and their migration across the embryonic midline. Neuron 11:209–220

    Article  CAS  PubMed  Google Scholar 

  • Smith CA (1961) Innervation pattern of the cochlea. The internal hair cell. Ann Otol Rhinol Laryngol 70:381–394

    Article  Google Scholar 

  • Sobkowicz HM (1992) The development of innervation in the organ of Corti. In: Romand R (ed) Development of auditory and vestibular systems 2. Elsevier, Amsterdam, pp 59–100

    Google Scholar 

  • Sobkowicz HM (2001) The development of the GABAergic innervation in the organ of corti of the mouse. CRC, Boca Raton, pp 117–136

    Google Scholar 

  • Sobkowicz HM, Emmerling MR (1989) Development of acetylcholinesterase-positive neuronal pathways in the cochlea of the mouse. J Neurocytol 18:209–224

    Article  CAS  PubMed  Google Scholar 

  • Song MR, Shirasaki R, Cai CL, Ruiz EC, Evans SM, Lee SK, Pfaff SL (2006) T-Box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development 133:4945–4955

    Article  CAS  PubMed  Google Scholar 

  • Spoendlin H (1966) The organization of the cochlear receptor. Fortschr Hals Nasen Ohrenheilkd 13:1–227

    CAS  PubMed  Google Scholar 

  • Studer M (2001) Initiation of facial motoneurone migration is dependent on rhombomeres 5 and 6. Development (Cambridge, UK) 128:3707–3716

    Article  CAS  Google Scholar 

  • Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384: 630–634

    Article  CAS  PubMed  Google Scholar 

  • Tiveron MC, Pattyn A, Hirsch MR, Brunet JF (2003) Role of Phox2b and Mash1 in the generation of the vestibular efferent nucleus. Dev Biol 260:46–57

    Article  CAS  PubMed  Google Scholar 

  • Usami S, Igarashi M, Thompson GC (1987) GABA-like immunoreactivity in the squirrel monkey vestibular endorgans. Brain Res 417:367–370

    Article  CAS  PubMed  Google Scholar 

  • Vetter DE, Mugnaini E (1992) Distribution and dendritic features of three groups of rat olivocochlear neurons. A study with two retrograde cholera toxin tracers. Anat Embryol (Berl) 185:1–16

    Article  CAS  Google Scholar 

  • Vetter DE, Adams JC, Mugnaini E (1991) Chemically distinct rat olivocochlear neurons. Synapse 7:21–43

    Article  CAS  PubMed  Google Scholar 

  • Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, Brown MC, Saffiote-Kolman J, Heinemann SF, Elgoyhen AB (1999) Role of alpha9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23:93–103

    Article  CAS  PubMed  Google Scholar 

  • Wackym PA (1993) Ultrastructural organization of calcitonin gene-related peptide immunoreactive efferent axons and terminals in the vestibular periphery. Am J Otol 14:41–50

    CAS  PubMed  Google Scholar 

  • Wackym PA, Popper P, Lopez 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 161:159–181

    Article  CAS  PubMed  Google Scholar 

  • Whitlon DS, Sobkowicz HM (1989) GABA-like immunoreactivity in the cochlea of the developing mouse. J Neurocytol 18:505–518

    Article  CAS  PubMed  Google Scholar 

  • Whitlon DS, Zhang X, Pecelunas K, Greiner MA (1999) A temporospatial map of adhesive molecules in the organ of Corti of the mouse cochlea. J Neurocytol 28:955–968

    Article  CAS  PubMed  Google Scholar 

  • Willmann R, Fuhrer C (2002) Neuromuscular synaptogenesis: clustering of acetylcholine receptors revisited. Cell Mol Life Sci 59:1296–1316

    Article  CAS  PubMed  Google Scholar 

  • Wilson JL, Henson MM, Henson OW Jr (1991) Course and distribution of efferent fibers in the cochlea of the mouse. Hear Res 55:98–108

    Article  CAS  PubMed  Google Scholar 

  • Zidanic M (2002) Cholinergic innervation of the chick basilar papilla. J Comp Neurol 445:159–175

    Article  PubMed  Google Scholar 

  • Zuo J, Treadaway J, Buckner TW, Fritzsch B (1999) Visualization of alpha9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified bacterial artificial chromosome. Proc Natl Acad Sci USA 96:14100–14105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by several NIH/NIDCD funds to some of the authors. We are indebted to the editors for help in stimulating this review.

Author information

Authors and Affiliations

  1. Department of Biology, University of Iowa, Iowa City, IA, 52242, USA

    Bernd Fritzsch

Authors
  1. Dwayne Simmons
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeremy Duncan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dominique Crapon de Caprona
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernd Fritzsch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Fritzsch .

Editor information

Editors and Affiliations

  1. Program in Neuroscience, Garvan Institute of Medical Research, 384 Victoria St., Level 7, Darlinghurst, NSW2010, Australia

    David K. Ryugo

  2. Parmly Hearing Institute, Loyola University Chicago, 6525 N. Sheridan Rd., Chicago, 60626, Illinois, USA

    Richard R. Fay

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Simmons, D., Duncan, J., de Caprona, D.C., Fritzsch, B. (2011). Development of the Inner Ear Efferent 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_7

Download citation

Publish with us

Policies and ethics

Search

Navigation