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.
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Arnesen AR (1984) Fibre population of the vestibulocochlear anastomosis in humans. Acta Otolaryngol 98:501–518
Arnesen AR, Osen KK (1984) Fibre spectrum of the vestibulo-cochlear anastomosis in the cat. Acta Otolaryngol 98:255–269
Aschoff A, Ostwald J (1987) Different origins of cochlear efferents in some bat species, rats, and guinea pigs. J Comp Neurol 264:56–72
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
Benson TE, Brown MC (1990) Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus. J Comp Neurol 295:52–70
Benson TE, Brown MC (1996) Synapses from medial olivocochlear branches in the inferior vestibular nucleus. J Comp Neurol 372:176–188
Benson TE, Brown MC (2006) Ultrastructure of synaptic input to medial olivocochlear neurons. J Comp Neurol 499:244–257
Bishop AL, Henson OW Jr (1987) The efferent cochlear projections of the superior olivary complex in the mustached bat. Hear Res 31:175–182
Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47–67
Brown MC (1987a) Morphology of labeled efferent fibers in the guinea pig cochlea. J Comp Neurol 260:605–618
Brown MC (1987b) Morphology of labeled afferent fibers in the guinea pig cochlea. J Comp Neurol 260:591–604
Brown MC (1989) Morphology and response properties of single olivocochlear fibers in the guinea pig. Hear Res 40:93–110
Brown MC (1993) Fiber pathways and branching patterns of biocytin-labeled olivocochlear neurons in the mouse brainstem. J Comp Neurol 337:600–613
Brown MC (2001) Response adaptation of medial olivocochlear neurons is minimal. J Neurophysiol 86:2381–2392
Brown MC (2002) Cochlear projections of single medial olivocochlear (MOC) axons in the guinea pig. ARO Absts 25:310
Brown MC, Levine JL (2008) Dendrites of medial olivocochlear (MOC) neurons in mouse. Neuroscience 154:147–159
Brown MC, Vetter DE (2008) Olivocochlear somata and central branches are normal in α9 knockout mice. J Assoc Res Otolaryngol 10:64–75
Brown MC, Liberman MC, Benson TE, Ryugo DK (1988) Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278:591–603
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
Campbell JP, Henson MM (1988) Olivocochlear neurons in the brainstem of the mouse. Hear Res 35:271–274
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
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
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
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
Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol (Berl) 175:35–52
Fujino K, Oertel D (2001) Cholinergic modulation of stellate cells in the mammalian ventral cochlear nucleus. J Neurosci 21:7372–7383
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
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
Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of the guinea pig. Anat Embryol 182:123–149
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
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
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
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
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
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
Kujawa S, Liberman MC (2001) Effects of olivocochlear feedback on distortion product otoacoustic emissions in guinea pig. J Assoc Res Otolaryngol 2:268–278
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
Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36
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
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
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
Matsuzaki M (2007) Factors critical for the plasticity of dendritic spines and memory storage. Neurosci Rev 57:1–9
Moore JK, Osen KK (1979) The cochlear nuclei in man. Am J Anat 154:393–418
Mulders WHAM, Robertson D (2000a) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hear Res 144:65–72
Mulders WHAM, Robertson D (2000b) Morphological relationships of peptidergic and noradrenergic nerve terminals to olivocochlear neurones in the rat. Hear Res 144:53–64
Mulders WHAM, Robertson D (2005) Catecholaminergic innervation of guinea pig superior olivary complex. J Chem Neuroanat 30:230–242
Mulders WHAM, Harvey AR, Robertson D (2007) Electrically-evoked responses in onset chopper neurons in guinea pig cochlear nucleus. J Neurophysiol 97:3288–3297
Nadol JB Jr (1988) Comparative anatomy of the cochlea and auditory nerve in mammals. Hear Res 34:253–266
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
Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–484
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
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 99:61–94
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
Robertson D, Gummer M (1985) Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear Res 20:63–77
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
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
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
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
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
Sánchez-González MA, Warr WB, López DE (2003) Anatomy of olivocochlear neurons in the hamster studied with FluoroGold. Hear Res 185:65–76
Schuknecht HF, Nomura Y (1965) The efferent fibers in the cochlea. Ann Otol Rhinol Laryngol 74:289–303
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
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
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
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
Spoendlin H (1971) Degeneration behaviour of the cochlear nerve. Arch Klin Exp Ohren Nasen Kehlkopfheilkd 200:275–291
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
Thiers FA, Burgess BJ, Nadol JB Jr (2002) Axodendritic and dendrodendritic synapses within outer spiral bundles in a human. Hear Res 164:97–104
Thompson GC, Thompson AM (1986) Olivocochlear neurons in the squirrel monkey brainstem. J Comp Neurol 254:246–258
Thompson AM, Thompson GC (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303:267–285
Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–412
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
Uchizono K (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature (Lond) 207:642–643
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
Vetter DE, Adams JC, Mugnaini E (1991) Chemically distinct rat olivocochlear neurons. Synapse 7:21–43
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
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
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
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
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
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
Warr WB, Guinan JJ Jr (1979) Efferent innervation of the organ of Corti: Two separate systems. Brain Res 173:152–155
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
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
Warren EH III, Liberman MC (1989) Effects of contralateral sound on auditory-nerve responses I. Contributions of cochlear efferents. Hear Res 37:89–104
White JS (1984) Fine structure of medial olivocochlear neurons in the rat. Soc Neurosci Abstr 10:393
White JS (1986) Differences in the ultrastructure of labyrinthine efferent neurons in the albino rat. ARO Abstr 9:34–35
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
Yao W, Godfrey DA (1999) Immunolocalization of alpha4 and alpha7 subunits of nicotinic receptor in rat cochlear nucleus. Hear Res 128:97–102
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
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.
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
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
Download citation
DOI: https://doi.org/10.1007/978-1-4419-7070-1_2
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)
