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Anatomy of Olivocochlear Neurons

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

Abstract

Hair cell receptors for the hearing and balance organs, and the lateral line, are unique among the senses by receiving an efferent innervation of the periphery. Olivocochlear (OC) neurons supply this efferent innervation, and they are the most peripheral of the many descending neural systems of the central auditory pathway (see Schofield, Chap. 9). OC neurons are named by their origins in the superior olivary complex and terminations in the cochlea (Fig. 2.1). In the cochlea, they innervate the hair cells and auditory-nerve fibers. This chapter mainly covers the new ground on OC anatomy in mammals since Warr’s (1992) comprehensive chapter on this topic about 15 years ago. Since that time, there is even stronger evidence for the separate innervation of the periphery by the two major groups of OC neurons. It is also now clear that both of these groups consist of distinct subgroups. There is additional information on the reflex pathways leading up to OC neurons that enables their response to sound. Overall, this anatomy may help to define the functions that OC neurons perform in the sense of hearing.

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References

  • Arnesen AR (1984) Fibre population of the vestibulocochlear anastomosis in humans. Acta Otolaryngol 98:501–518

    CAS  PubMed  Google Scholar 

  • Arnesen AR, Osen KK (1984) Fibre spectrum of the vestibulo-cochlear anastomosis in the cat. Acta Otolaryngol 98:255–269

    CAS  PubMed  Google Scholar 

  • Aschoff A, Ostwald J (1987) Different origins of cochlear efferents in some bat species, rats, and guinea pigs. J Comp Neurol 264:56–72

    CAS  PubMed  Google Scholar 

  • Azeredo WJ, Kliment ML, Morley BJ, Relkin E, Slepecky NB, Sterns A, Warr WB, Weekly JM, Woods CI (1999) Olivocochlear neurons in the chinchilla: A retrograde fluorescent labelling study. Hear Res 134:57–70

    CAS  PubMed  Google Scholar 

  • Benson TE, Brown MC (1990) Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus. J Comp Neurol 295:52–70

    CAS  PubMed  Google Scholar 

  • Benson TE, Brown MC (1996) Synapses from medial olivocochlear branches in the inferior vestibular nucleus. J Comp Neurol 372:176–188

    CAS  PubMed  Google Scholar 

  • Benson TE, Brown MC (2006) Ultrastructure of synaptic input to medial olivocochlear neurons. J Comp Neurol 499:244–257

    PubMed  Google Scholar 

  • Bishop AL, Henson OW Jr (1987) The efferent cochlear projections of the superior olivary complex in the mustached bat. Hear Res 31:175–182

    CAS  PubMed  Google Scholar 

  • Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47–67

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Brown MC (1987b) Morphology of labeled afferent fibers in the guinea pig cochlea. J Comp Neurol 260:591–604

    CAS  PubMed  Google Scholar 

  • Brown MC (1989) Morphology and response properties of single olivocochlear fibers in the guinea pig. Hear Res 40:93–110

    CAS  PubMed  Google Scholar 

  • Brown MC (1993) Fiber pathways and branching patterns of biocytin-labeled olivocochlear neurons in the mouse brainstem. J Comp Neurol 337:600–613

    CAS  PubMed  Google Scholar 

  • Brown MC (2001) Response adaptation of medial olivocochlear neurons is minimal. J Neurophysiol 86:2381–2392

    CAS  PubMed  Google Scholar 

  • Brown MC (2002) Cochlear projections of single medial olivocochlear (MOC) axons in the guinea pig. ARO Absts 25:310

    Google Scholar 

  • Brown MC, Levine JL (2008) Dendrites of medial olivocochlear (MOC) neurons in mouse. Neuroscience 154:147–159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown MC, Vetter DE (2008) Olivocochlear somata and central branches are normal in α9 knockout mice. J Assoc Res Otolaryngol 10:64–75

    PubMed  PubMed Central  Google Scholar 

  • Brown MC, Liberman MC, Benson TE, Ryugo DK (1988) Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278:591–603

    CAS  PubMed  Google Scholar 

  • Brown MC, de Venecia RK, Guinan JJ Jr (2003) Responses of medial olivocochlear (MOC) neurons: Specifying the central pathways of the MOC reflex. Exp Brain Res 153:491–498

    CAS  PubMed  Google Scholar 

  • Campbell JP, Henson MM (1988) Olivocochlear neurons in the brainstem of the mouse. Hear Res 35:271–274

    CAS  PubMed  Google Scholar 

  • Darrow KN, Simons EJ, Dodds L, Liberman MC (2006) Dopaminergic innervation of the mouse inner ear: Evidence for a separate cytochemical group of cochlear efferent fibers. J Comp Neurol 498:403–414

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Boer E, Thornton AR (2008) Neural correlates of perceptual learning in the auditory brainstem: efferent activity predicts and reflects improvement at a speech-in-noise discrimination task. J Neurosci 28:4929–4937

    PubMed  PubMed Central  Google Scholar 

  • de Venecia RK, Liberman MC, Guinan JJ Jr, Brown MC (2005) Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus. J Comp Neurol 487: 345–360

    PubMed  PubMed Central  Google Scholar 

  • Doucet JR, Ryugo DK (2003) Axonal pathways to the lateral superior olive labeled with biotinylated dextran amine injections in the dorsal cochlear nucleus in rats. J Comp Neurol 461:452–465

    PubMed  Google Scholar 

  • Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol (Berl) 175:35–52

    CAS  Google Scholar 

  • Fujino K, Oertel D (2001) Cholinergic modulation of stellate cells in the mammalian ventral cochlear nucleus. J Neurosci 21:7372–7383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guinan JJ Jr, Warr WB, Norris BE (1983) Differential olivocochlear projections from lateral vs. medial zones of the superior olivary complex. J Comp Neurol 221:358–370

    PubMed  Google Scholar 

  • Guinan JJ Jr, Warr WB, Norris BE (1984) Topographic organization of the olivocochlear projections from the lateral and medial zones of the superior olivary complex. J Comp Neurol 226:21–27

    PubMed  Google Scholar 

  • Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of the guinea pig. Anat Embryol 182:123–149

    CAS  PubMed  Google Scholar 

  • Happe HK, Morely BJ (1998) Nicotinic acetylcholine receptors in rat cochlear nucleus: [125I]-a-bungarotoxin receptor autoradiography and in situ receptor autoradiography of a7 nAChR subunit mRNA. J Comp Neurol 397:163–180

    CAS  PubMed  Google Scholar 

  • Helfert RH, Schwartz IR, Ryan AF (1988) Ultrastructural characterization of gerbil olivocochlear neurons based on differential uptake of 3H-d-aspartic acid and a wheatgerm agglutinin-horseradish peroxidase conjugate from the cochlea. J Neurosci 8:3111–3123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horvath M, Kraus KS, Illing R-B (2000) Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat. J Comp Neurol 422:95–105

    CAS  PubMed  Google Scholar 

  • Horvath M, Ribari O, Repassy G, Toth IE, Boldogkoi Z, Palkovits M (2003) Intracochlear injection of pseudorabies virus labels descending auditory and monoaminerg projections to olivocochlear cells in guinea pig. Eur J Neurosci 18:1439–1447

    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

    CAS  PubMed  Google Scholar 

  • Kiang NYS, Rho JM, Northrop CC, Liberman MC, Ryugo DK (1982) Hair-cell innervation by spiral ganglion cells in adult cats. Science 217:175–177

    CAS  PubMed  Google Scholar 

  • Kujawa S, Liberman MC (2001) Effects of olivocochlear feedback on distortion product otoacoustic emissions in guinea pig. J Assoc Res Otolaryngol 2:268–278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liberman MC (1980) Efferent synapses in the inner hair cell area of the cat cochlea: An electron microscopic study of serial sections. Hear Res 3:189–204

    CAS  PubMed  Google Scholar 

  • Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36

    CAS  PubMed  Google Scholar 

  • Liberman MC, Guinan JJ Jr (1998) Feedback control of the auditory periphery: Anti-masking effects of middle ear muscles vs. olivocochlear efferents. J Commun Disord 31:471–483

    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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuzaki M (2007) Factors critical for the plasticity of dendritic spines and memory storage. Neurosci Rev 57:1–9

    Google Scholar 

  • Moore JK, Osen KK (1979) The cochlear nuclei in man. Am J Anat 154:393–418

    CAS  PubMed  Google Scholar 

  • Mulders WHAM, Robertson D (2000a) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hear Res 144:65–72

    CAS  PubMed  Google Scholar 

  • Mulders WHAM, Robertson D (2000b) Morphological relationships of peptidergic and noradrenergic nerve terminals to olivocochlear neurones in the rat. Hear Res 144:53–64

    CAS  PubMed  Google Scholar 

  • Mulders WHAM, Robertson D (2005) Catecholaminergic innervation of guinea pig superior olivary complex. J Chem Neuroanat 30:230–242

    CAS  PubMed  Google Scholar 

  • Mulders WHAM, Harvey AR, Robertson D (2007) Electrically-evoked responses in onset chopper neurons in guinea pig cochlear nucleus. J Neurophysiol 97:3288–3297

    PubMed  Google Scholar 

  • Nadol JB Jr (1988) Comparative anatomy of the cochlea and auditory nerve in mammals. Hear Res 34:253–266

    PubMed  Google Scholar 

  • Oliver DL (1987) Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: Possible substrates for binaural interaction. J Comp Neurol 264:24–46

    CAS  PubMed  Google Scholar 

  • Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–484

    CAS  PubMed  Google Scholar 

  • Osen KK, Mugnaini E, Dahl A-L, 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 

  • Rasmussen GL (1946) The olivary peduncle and other fiber connections of the superior olivary complex. J Comp Neurol 84:141–219

    CAS  PubMed  Google Scholar 

  • Rasmussen GL (1953) Further observations of the efferent cochlear bundle. J Comp Neurol 99:61–94

    CAS  PubMed  Google Scholar 

  • Rhode WS, Oertel D, Smith PH (1983) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J Comp Neurol 213:448–463

    CAS  PubMed  Google Scholar 

  • Robertson D, Gummer M (1985) Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear Res 20:63–77

    CAS  PubMed  Google Scholar 

  • Robertson D, Winter IM (1988) Cochlear nucleus inputs to olivocochlear neurones revealed by combined anterograde and retrograde labelling in the guinea pig. Brain Res 462:47–55

    CAS  PubMed  Google Scholar 

  • Robertson D, Cole KS, Corbett K (1987a) Quantitative estimate of bilaterally projecting medial olivocochlear neurons in the guinea pig brainstem. Hear Res 27:177–181

    CAS  PubMed  Google Scholar 

  • Robertson D, Anderson C-J, Cole KS (1987b) Segregation of efferent projections to different turns of the guinea pig cochlea. Hear Res 25:69–76

    CAS  PubMed  Google Scholar 

  • Rouiller EM, Ryugo DK (1984) Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J Comp Neurol 225:167–186

    CAS  PubMed  Google Scholar 

  • Ryan AF, Keithley EM, Wang Z-X, Schwartz IR (1990) Collaterals from lateral and medial olivocochlear efferent neurons innervate different regions of the cochlear nucleus and adjacent brainstem. J Comp Neurol 300:572–582

    CAS  PubMed  Google Scholar 

  • Sánchez-González MA, Warr WB, López DE (2003) Anatomy of olivocochlear neurons in the hamster studied with FluoroGold. Hear Res 185:65–76

    PubMed  Google Scholar 

  • Schuknecht HF, Nomura Y (1965) The efferent fibers in the cochlea. Ann Otol Rhinol Laryngol 74:289–303

    PubMed  Google Scholar 

  • Smith PH, Joris PX, Carney LH, Yin TCT (1991) Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304:387–407

    CAS  PubMed  Google Scholar 

  • Smith PH, Joris PX, Banks MI, Yin TCT (1993) Responses of cochlear nucleus cells and projections of their axons. In: Merchan MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The mammalian cochlear nuclei: Organization and function. Plenum Press, New York, pp 349–360

    Google Scholar 

  • Spangler KM, White JS, Warr WB (1986) Electron microscopic features of axon terminals on olivocochlear neurons in the cat. Assoc Res Otolaryngol Abstr 9:37–38

    Google Scholar 

  • Spirou GA, Brownell WE, Zidanic M (1990) Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J Neurophysiol 63:1169–1190

    CAS  PubMed  Google Scholar 

  • Spoendlin H (1971) Degeneration behaviour of the cochlear nerve. Arch Klin Exp Ohren Nasen Kehlkopfheilkd 200:275–291

    CAS  PubMed  Google Scholar 

  • Stopp PE (1983) The distribution of the olivocochlear bundle and its possible role in frequency/intensity coding. In: Klinke R, Hartmann R (eds) Hearing-physiological bases and physchophysics. Springer, Berlin, pp 176–179

    Google Scholar 

  • Thiers FA, Burgess BJ, Nadol JB Jr (2002) Axodendritic and dendrodendritic synapses within outer spiral bundles in a human. Hear Res 164:97–104

    PubMed  Google Scholar 

  • Thompson GC, Thompson AM (1986) Olivocochlear neurons in the squirrel monkey brainstem. J Comp Neurol 254:246–258

    CAS  PubMed  Google Scholar 

  • Thompson AM, Thompson GC (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303:267–285

    CAS  PubMed  Google Scholar 

  • Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–412

    CAS  PubMed  Google Scholar 

  • Thompson AM, Thompson GC (1995) Light microscopic evidence of serotoninergic projections to olivocochlear neurons in the bush baby (Otolemur garnettii). Brain Res 695:263–266

    CAS  PubMed  Google Scholar 

  • Uchizono K (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature (Lond) 207:642–643

    CAS  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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Vetter DE, Saldana E, Mugnaini E (1993) Input from the inferior colliculus to medial olivocochlear neurons in the rat: A double label study with PHA-L and cholera toxin. Hear Res 70:173–186

    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 a9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23:93–103

    CAS  PubMed  Google Scholar 

  • Wang X, Robertson D (1997a) Effects of bioamines and peptides on neurones in the ventral nucleus of the trapezoid body and rostral periolivary regions of the rat superior olivary complex: An in vitro investigation. Hear Res 106:20–28

    CAS  PubMed  Google Scholar 

  • Wang X, Robertson D (1997b) Two types of actions of noradrenaline on identified auditory efferent neurons in rat brainstem slices. J Neurophysiol 78:1800–1810

    CAS  PubMed  Google Scholar 

  • Warr WB (1975) Olivocochlear and vestibular efferent neurons of the feline brainstem: Their location, morphology, and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol 161:159–182

    CAS  PubMed  Google Scholar 

  • Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: Neuroanatomy. Springer, New York, pp 410–448

    Google Scholar 

  • Warr WB, Guinan JJ Jr (1979) Efferent innervation of the organ of Corti: Two separate systems. Brain Res 173:152–155

    CAS  PubMed  Google Scholar 

  • Warr WB, Beck Boche JE, Neely ST (1997) Efferent innervation of the inner hair cell region: Origins and terminations of two lateral olivocochlear systems. Hear Res 108:89–111

    CAS  PubMed  Google Scholar 

  • Warr WB, Boche JEB, Ye Y, Kim DO (2002) Organization of olivocochlear neurons in the cat studied with the retrograde tracer cholera toxin-B. J Assoc Res Otolaryngol 3:457–478

    PubMed  PubMed Central  Google Scholar 

  • Warren EH III, Liberman MC (1989) Effects of contralateral sound on auditory-nerve responses I. Contributions of cochlear efferents. Hear Res 37:89–104

    PubMed  Google Scholar 

  • White JS (1984) Fine structure of medial olivocochlear neurons in the rat. Soc Neurosci Abstr 10:393

    Google Scholar 

  • White JS (1986) Differences in the ultrastructure of labyrinthine efferent neurons in the albino rat. ARO Abstr 9:34–35

    Google Scholar 

  • Winter IM, Robertson D, Cole KS (1989) Descending projections from auditory brainstem nuclei to the cochlea and cochlear nucleus of the guinea pig. J Comp Neurol 280:143–157

    CAS  PubMed  Google Scholar 

  • Yao W, Godfrey DA (1999) Immunolocalization of alpha4 and alpha7 subunits of nicotinic receptor in rat cochlear nucleus. Hear Res 128:97–102

    CAS  PubMed  Google Scholar 

  • Ye Y, Machado DG, Kim DO (2000) Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J Comp Neurol 420:127–138

    CAS  PubMed  Google Scholar 

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Acknowledgments

I thank Dr. M. Charles Liberman for comments on the manuscript and Ms. Marie Drottar for assistance with the figures. This work was Supported by NIH grant DCD 01089.

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Correspondence to M. Christian Brown .

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Brown, M.C. (2011). Anatomy of Olivocochlear Neurons. 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_2

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