Abstract
Electrical stimulation of the inferior colliculus (IC) has been shown to result in suppression of cochlear output, due to activation of the medial olivocochlear system. This auditory efferent system originates in the brainstem and terminates on the outer hair cells in the cochlea. Recently, excitatory effects of IC stimulation have also been reported, both on cochlear gross potentials and on primary auditory afferents. It has been hypothesized that this excitation is due to co-activation of the lateral olivocochlear system, which synapses on the primary auditory afferent fibres contacting the inner hair cells. If stimulation of the IC leads to the activation of both the medial and lateral olivocochlear system, resulting in a mixture of inhibitory and excitatory effects in the cochlea, then removal of the inhibitory effects, by blocking the medial system, should lead to more pronounced excitatory effects out in the periphery. To investigate this hypothesis, we recorded the effect of IC stimulation on cochlear gross potentials as well as on single auditory primary afferents in guinea pigs following block of the medial olivocochlear system with gentamicin. We found that administration of gentamicin, whether intraperitoneally or by intracochlear perfusion, blocked all effects of IC stimulation, whether inhibitory or excitatory. These data strongly suggest that all effects observed after IC stimulation, both inhibitory as well as excitatory, are due to the activation of the medial olivocochlear system.
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References
Alder VA, Johnstone BM (1978) A new approach to the guinea pig auditory nerve. J Acoust Soc Am 64:684–687
Aran JM, Chappert C, Dulon D, Erre JP, Aurousseau C (1995) Uptake of amikacin by hair cells of the guinea pig cochlea and vestibule and ototoxicity: comparison with gentamicin. Hear Res 82:179–183
Avan P, Erre JP, da Costa DL, Aran JM, Popelar J (1996) The efferent-mediated suppression of otoacoustic emissions in awake guinea pigs and its reversible blockage by gentamicin. Exp Brain Res 109:9–16
Beyerl BD (1978) Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Res 145:209–223
Blanchet C, Erostegui C, Sugasawa M, Dulon D (2000) Gentamicin blocks ACh-evoked K+ current in guinea-pig outer hair cells by impairing Ca2+ entry at the cholinergic receptor. J Physiol 525(Pt3):641–654
Brown MC, Nuttall AL (1984) Efferent control of cochlear inner hair cell responses in the guinea-pig. J Physiol 354:625–646
Caicedo A, Herbert H (1993) Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J Comp Neurol 328:377–392
Coleman JR, Clerici WJ (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262:215–226
Desmedt J (1962) Auditory-evoked potentials from cochlea to cortex as influenced by activation of the efferent olivocochlear bundle. J Acoust Soc Am 34:1478–1496
Dolan DF, Guo MH, Nuttall AL (1997) Frequency-dependent enhancement of basilar membrane velocity during olivocochlear bundle stimulation. J Acoust Soc Am 102:3587–3596
Dulon D, Zajic G, Aran JM, Schacht J (1989) Aminoglycoside antibiotics impair calcium entry but not viability and motility in isolated cochlear outer hair cells. J Neurosci Res 24:338–346
Dulon D, Hiel H, Aurousseau C, Erre JP, Aran JM (1993) Pharmacokinetics of gentamicin in the sensory hair cells of the organ of Corti: rapid uptake and long term persistence. C R Acad Sci III 316:682–687
Dulon D, Sugasawa M, Blanchet C, Erostegui C (1995) Direct measurements of Ca(2+)-activated K+ currents in inner hair cells of the guinea-pig cochlea using photolabile Ca2+ chelators. Pflugers Arch 430:365–373
Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol (Berl) 175:35–52
Felix D, Ehrenberger K (1992) The efferent modulation of mammalian inner hair cell afferents. Hear Res 64:1–5
Gaborjan A, Halmos G, Repassy G, Vizi ES (2001) A new aspect of aminoglycoside ototoxicity: impairment of cochlear dopamine release. Neuroreport 12:3327–3330
Gao E, Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc Natl Acad Sci USA 97:8081–8086
Giraud AL, Collet L, Chery-Croze S, Magnan J, Chays A (1995) Evidence of a medial olivocochlear involvement in contralateral suppression of otoacoustic emissions in humans. Brain Res 705:15–23
Groff JA, Liberman MC (2003) Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J Neurophysiol 90:3178–3200
Guinan JJ Jr (1996) Physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds) The cochlea, Springer, Berlin Heidelberg New York, pp 435–502
Guinan JJ Jr, Gifford ML (1988) Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. I. Rate-level functions. Hear Res 33:97–113
Guinan JJ Jr, Stankovic KM (1996) Medial efferent inhibition produces the largest equivalent attenuations at moderate to high sound levels in cat auditory-nerve fibers. J Acoust Soc Am 100:1680–1690
Guitton MJ, Avan P, Puel JL, Bonfils P (2004) Medial olivocochlear efferent activity in awake guinea pigs. Neuroreport 15:1379–1382
Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103–122
Hiel H, Erre JP, Aurousseau C, Bouali R, Dulon D, Aran JM (1993) Gentamicin uptake by cochlear hair cells precedes hearing impairment during chronic treatment. Audiology 32:78–87
Johnstone JR, Alder VA, Johnstone BM, Robertson D, Yates GK (1979) Cochlear action potential threshold and single unit thresholds. J Acoust Soc Am 65:254–257
Kawase T, Liberman MC (1993) Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. J Neurophysiol 70:2519–2532
Kemp DT, Souter M (1988) A new rapid component in the cochlear response to brief electrical efferent stimulation: CM and otoacoustic observations. Hear Res 34:49–62
Le Prell CG, Shore SE, Hughes LF, Bledsoe SC Jr (2003) Disruption of lateral efferent pathways: functional changes in auditory evoked responses. J Assoc Res Otolaryngol 4:276–290
Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455
Liberman MC (1990) Effects of chronic cochlear de-efferentation on auditory-nerve response. Hear Res 49:209–223
Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36
Lima da Costa D, Erre JP, Aran JM (1998) Aminoglycoside ototoxicity and the medial efferent system: I. Comparison of acute and chronic gentamicin treatments. Audiology 37:151–161
Ma X, Suga N (2001) Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proc Natl Acad Sci USA 98:14060–14065
Malmierca MS, Le Beau FE, Rees A (1996) The topographical organization of descending projections from the central nucleus of the inferior colliculus in guinea pig. Hear Res 93:167–180
McDowell B (1982) Patterns of cochlear degeneration following gentamicin administration in both old and young guinea pigs. Br J Audiol 16:123–129
Mulders WH, Robertson D (2000) Effects on cochlear responses of activation of descending pathways from the inferior colliculus. Hear Res 149:11–23
Mulders WH, Robertson D (2002) Inputs from the cochlea and the inferior colliculus converge on olivocochlear neurones. Hear Res 167:206–213
Mulders WH, Robertson D (2005) Diverse responses of single auditory afferent fibres to electrical stimulation of the inferior colliculus in guinea-pig. Exp Brain Res 160:235–244
Ota Y, Oliver DL, Dolan DF (2004) Frequency-specific effects on cochlear responses during activation of the inferior colliculus in the Guinea pig. J Neurophysiol 91:2185–2193
Popelar J, Mazelova J, Syka J (2002) Effects of electrical stimulation of the inferior colliculus on 2f1–f2 distortion product otoacoustic emissions in anesthetized guinea pigs. Hear Res 170:116–126
Popelar J, Nwabueze-Ogbo FC, Syka J (2003) Changes in neuronal activity of the inferior colliculus in rat after temporal inactivation of the auditory cortex. Physiol Res 52:615–628
Rajan R (1988a) Effect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. I. Dependence on electrical stimulation parameters. J Neurophysiol 60:549–568
Rajan R (1988b) Effect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. II. Dependence on the level of temporary threshold shifts. J Neurophysiol 60:569–579
Rajan R (2001a) Cochlear outer-hair-cell efferents and complex-sound-induced hearing loss: protective and opposing effects. J Neurophysiol 86:3073–3076
Rajan R (2001b) Unilateral hearing losses alter loud sound-induced temporary threshold shifts and efferent effects in the normal-hearing ear. J Neurophysiol 85:1257–1269
Robertson D (1985) Brainstem location of efferent neurones projecting to the guinea pig cochlea. Hear Res 20:79–84
Robertson D, Cole KS, Corbett K (1987) Quantitative estimate of bilaterally projecting medial olivocochlear neurones in the guinea pig brainstem. Hear Res 27:177–181
Rothlin CV, Katz E, Verbitsky M, Vetter DE, Heinemann SF, Elgoyhen AB (2000) Block of the alpha9 nicotinic receptor by ototoxic aminoglycosides. Neuropharmacology 39:2525–2532
Ruel J, Nouvian R, Gervais d’Aldin C, Pujol R, Eybalin M, Puel JL (2001) Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur J Neurosci 14:977–986
Ruggero MA, Rich NC (1991) Furosemide alters organ of corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane. J Neurosci 11:1057–1067
Saldana E, Feliciano M, Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371:15–40
Schofield BR, Cant NB (1999) Descending auditory pathways: projections from the inferior colliculus contact superior olivary cells that project bilaterally to the cochlear nuclei. J Comp Neurol 409:210–223
Sheppard WM, Wanamaker HH, Pack A, Yamamoto S, Slepecky N (2004) Direct round window application of gentamicin with varying delivery vehicles: a comparison of ototoxicity. Otolaryngol Head Neck Surg 131:890–896
Smith DW, Erre JP, Aran JM (1994) Rapid, reversible elimination of medial olivocochlear efferent function following single injections of gentamicin in the guinea pig. Brain Res 652:243–248
Syka J, Popelar J (1984) Inferior colliculus in the rat: neuronal responses to stimulation of the auditory cortex. Neurosci Lett 51:235–240
Sziklai I, He DZ, Dallos P (1996) Effect of acetylcholine and GABA on the transfer function of electromotility in isolated outer hair cells. Hear Res 95:87–99
Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–412
Torterolo P, Zurita P, Pedemonte M, Velluti RA (1998) Auditory cortical efferent actions upon inferior colliculus unitary activity in the guinea pig. Neurosci Lett 249:172–176
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
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, Guinan JJ Jr (1979) Efferent innervation of the organ of corti: two separate systems. Brain Res 173:152–155
Warren EH III, Liberman MC (1989) Effects of contralateral sound on auditory-nerve responses. II. Dependence on stimulus variables. Hear Res 37:105–121
White JS, Warr WB (1983) The dual origins of the olivocochlear bundle in the albino rat. J Comp Neurol 219:203–214
Wiederhold ML, Kiang NY (1970) Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. J Acoust Soc Am 48:950–965
Winer JA, Larue DT, Diehl JJ, Hefti BJ (1998) Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400:147–174
Winslow RL, Sachs MB (1987) Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. J Neurophysiol 57:1002–1021
Yan J, Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci 16:119–128
Yan W, Suga N (1998) Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat Neurosci 1:54–58
Yoshida N, Liberman MC, Brown MC, Sewell WF (1999) Gentamicin blocks both fast and slow effects of olivocochlear activation in anesthetized guinea pigs. J Neurophysiol 82:3168–3174
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
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This study was supported by grants from the National Health and Medical Research Council, the Medical Health and Research Infrastructure Fund (WA) and The University of Western Australia.
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Mulders, W.H.A.M., Robertson, D. Gentamicin abolishes all cochlear effects of electrical stimulation of the inferior colliculus. Exp Brain Res 174, 35–44 (2006). https://doi.org/10.1007/s00221-006-0418-6
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DOI: https://doi.org/10.1007/s00221-006-0418-6