Lateral and medial efferents: a double neurochemical mechanism to protect and regulate inner and outer hair cell function in the cochlea.

In the mammalian cochlea, the two types of hair cells drastically differ in their anatomy and physiology. Each system receives a specific efferent control originating in the brainstem superior olivary complex. Inner hair cells are connected to the afferent type I ganglion neurons (comprising 95% of the auditory nerve) which postsynaptically receive the input of the lateral efferents. On the other hand, outer hair cells, whose electromotile properties are responsible for the active mechanism, are directly under medial efferent control. Neurochemically, both types of efferents are also well distinguished. The present paper reviews the efferent neurochemistry and pharmacology, with an emphasis on the protective roles of each system on cochlear function. The role of lateral efferent neurotransmitters such as enkephalins and dopamine in protecting the auditory nerve dendrites against excessive noise and/or excitotoxicity is especially addressed. The cholinergic medial efferents synapsing with the outer hair cells play a role in altering and/or modulating cochlear micromechanics. They could also be involved in a potentiating effect on aminoglycoside ototoxicity.

[1]  M. Liberman The olivocochlear efferent bundle and susceptibility of the inner ear to acoustic injury. , 1991, Journal of neurophysiology.

[2]  R. Pujol,et al.  Localisation of functional muscarinic receptors in the rat cochlea: evidence for efferent presynaptic autoreceptors , 1993, Brain Research.

[3]  S. Kujawa,et al.  Contralateral sound suppresses distortion product otoacoustic emissions through cholinergic mechanisms , 1993, Hearing Research.

[4]  R. Altschuler,et al.  Tyrosine hydroxylase immunoreactivity identifies possible catecholaminergic fibers in the organ of Corti , 1987, Hearing Research.

[5]  G. Rebillard,et al.  Effect of noise level on the Met-enkephalin content of the guinea pig cochlea , 1987, Brain Research.

[6]  D. Robertson,et al.  Segregation of efferent projections to different turns of the guinea pig cochlea , 1987, Hearing Research.

[7]  P. Gil-Loyzaga,et al.  Piribedil could modify dopamine turnover in cochleas under noise stimulation. , 1993, ORL; journal for oto-rhino-laryngology and its related specialties.

[8]  Tinnitus associated spontaneous otoacoustic emissions. Active outer hair cell movements as common origin? , 1990, Acta oto-laryngologica.

[9]  T Kawase,et al.  Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. , 1993, Journal of neurophysiology.

[10]  J. Puel,et al.  Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity , 1994, The Journal of comparative neurology.

[11]  Sally E. Williams,et al.  Three molecular steps of aminoglycoside ototoxicity demonstrated in outer hair cells , 1987, Hearing Research.

[12]  J. Puel,et al.  Pathophysiology of the glutamatergic synapses in the cochlea. , 1993, Acta oto-laryngologica.

[13]  R. Pujol,et al.  Localisation ultrastructurale des immunoréactions à un anticorps met-enképhaline dans l'organe de Corti , 1983 .

[14]  P A Fuchs,et al.  Cholinergic inhibition of short (outer) hair cells of the chick's cochlea , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Lionel Collet,et al.  Auditory selective attention in the human cochlea , 1994, Brain Research.

[16]  M. Eybalin,et al.  Dopaminergic lateral efferent innervation of the guinea-pig cochlea: Immunoelectron microscopy of catecholamine-synthesizing enzymes and effect of 6-hydroxydopamine , 1993, Neuroscience.

[17]  P. Gil-Loyzaga,et al.  HPLC detection of dopamine and noradrenaline in the cochlea of adult and developing rats. , 1989, Brain research. Developmental brain research.

[18]  S. Norton,et al.  Tinnitus and Otoacoustic Emissions: Is There a Link? , 1990, Ear and hearing.

[19]  N. Akaike,et al.  Cellular mechanism of acetylcholine‐induced response in dissociated outer hair cells of guinea‐pig cochlea. , 1993, The Journal of physiology.

[20]  G. Rebillard,et al.  Effect of contralateral sound stimulation on the distortion product 2F1-F2: evidence that the medial efferent system is involved. , 1990, The Journal of the Acoustical Society of America.

[21]  J. Puel,et al.  Implication of non‐NMDA and NMDA receptors in cochlear ischemia , 1992, Neuroreport.

[22]  T Kawase,et al.  Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. , 1993, Journal of neurophysiology.

[23]  M. Capps,et al.  Ototoxicity and the olivocochlear bundle , 1977, The Laryngoscope.

[24]  John J. Guinan,et al.  Efferent innervation of the organ of corti: two separate systems , 1979, Brain Research.

[25]  J. Bockaert,et al.  Opioid receptors inhibit the adenylate cyclase in guinea pig cochleas , 1987, Brain Research.

[26]  S. Pierce,et al.  Cochlear‐nucleus branches of thick (medial) olivocochlear fibers in the mouse: A cochaleotopic projection , 1991, The Journal of comparative neurology.

[27]  M. Drescher,et al.  Effect of Sound Stimulation at Several Levels on Concentrations of Primary Amines, Including Neurotransmitter Candidates, in Perilymph of the Guinea Pig Inner Ear , 1983, Journal of neurochemistry.

[28]  B. Kachar,et al.  Immunocytochemical localization of choline acetyltransferase-like immunoreactivity in the guinea pig cochlea , 1985, Brain Research.

[29]  N. Kiang,et al.  Central trajectories of type II spiral ganglion neurons , 1988, The Journal of comparative neurology.

[30]  P. Dallos The active cochlea , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R. Altschuler,et al.  Enkephalin-like immunoreactivity of olivocochlear nerve fibers in cochlea of guinea pig and cat. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Schacht,et al.  Motility of cochlear outer hair cells. , 1992, The American journal of otology.

[33]  W. Warr Organization of Olivocochlear Efferent Systems in Mammals , 1992 .

[34]  David T. Kemp,et al.  Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects , 1990, Hearing Research.

[35]  M. Eybalin,et al.  Neurotransmitters and neuromodulators of the mammalian cochlea. , 1993, Physiological reviews.

[36]  J F Ashmore,et al.  Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  J. Schacht Molecular mechanisms of drug-induced hearing loss , 1986, Hearing Research.

[38]  P. Plinkert,et al.  A nicotinic acetylcholine receptor-like α-bungarotoxin-binding site on outer hair cells , 1991, Hearing Research.

[39]  R. Pujol,et al.  Characterization of muscarinic binding sites in the adult and developing rat cochlea , 1993, Neurochemistry International.

[40]  Jean-Luc Puel,et al.  Selective attention modifies the active micromechanical properties of the cochlea , 1988, Brain Research.

[41]  L. Collet,et al.  Variability of the influence of a visual task on the active micromechanical properties of the cochlea , 1990, Brain Research.

[42]  R. D. Brown,et al.  Neomycin: ototoxicity and the cochlear efferents. , 1973, Acta oto-laryngologica.