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Benzodiazepines Alter Cochleo-Cochlear Loop in Humans

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Benzodiazepines Alter Cochleo-Cochlear Loop in Humans Hearing Research 121 (1998) 71^76 Benzodiazepines alter cochleo-cochlear loop in humans N. Morand a, E. Veuillet a;*, M.C. Gagnieu b, P. Lemoine c, L. Collet a a Laboratoire `Neurosciences et Systeémes Sensoriels', 3 place d'Arsonval, Pavillon U, Hoêpital Edouard Herriot, 69003 Lyon, France b Laboratoire de Pharmacologie, Hoêpital Edouard Herriot, Lyon, France c Uniteè Clinique de Psychiatrie Biologique, Le Vinatier, Bron, France Received 26 November 1997; revised 26 March 1998; accepted 7 April 1998 Abstract By using otoacoustic emission, we looked for change in outer hair cell (OHC) motile activity and medial olivocochlear (MOC) system inhibition due to benzodiazepine administration, a drug that is known to produce a pharmacological effect by interacting with GABAergic inhibitory neurotransmission. No effect was observed on OHC motile activity, in contrast benzodiazepines decreased MOC system effectiveness suggesting the existence of GABAergic fibers projecting onto the MOC system. z 1998 Elsevier Science B.V. All rights reserved. Key words: Gamma-aminobutyric acid; Outer hair cell; Olivocochlear e¡erent system; Otoacoustic emission 1. Introduction OHCs, principally acetylcholine (Ach) and the inhibi- tory neurotransmitter Q-aminobutyric acid (GABA) (for The organ of Corti is innervated by the olivocochlear review see Eybalin, 1993). Concerning GABA, several e¡erent system (Rasmussen, 1946), in which two sub- studies seem to prove the presence of GABAergic syn- components have been clearly distinguished (Warr, apses in the cochlea. The presence of GABA and glu- 1992; Warr and Guinan, 1979). The lateral olivo- tamic acid decarboxylase in ¢bers and e¡erent endings cochlear (LOC) system originates from lateral superior synapsing onto OHC bodies has been revealed by im- olivary neurons making synaptic contact with the a¡er- munocytochemistry data (Fex and Altschuler, 1984; ent inner radial ¢bers of the inner hair cell system. The Fex et al., 1986; Thompson et al., 1986; Eybalin et medial e¡erent system originates from the medial al., 1990). Furthermore, the presence of GABAA recep- superior olivary complex (SOC) or trapezoid body, tors in the outer cell membrane of isolated OHCs has synapsing with the basal pole of outer hair cells been demonstrated using monoclonal antibodies against (OHCs). the K- and L-subunits of GABAA receptors (Plinkert et Various neurotransmitters seem to be involved be- al., 1989). GABAA receptors are at the basal pole of tween the medial olivocochlear (MOC) system and the OHCs. GABA uptake by e¡erent endings has also been demonstrated (Schwartz and Ryan, 1983; Ryan et al., 1992). The action of GABA or agonists of GABA on OHC * Corresponding author. Tel.: +33 04 72 11 05 02; mechanisms has been studied, leading to contradictory Fax: +33 04 72 11 05 04; E-mail: [email protected] conclusions. In vitro, OHC hyperpolarization was ob- served after GABA application; this hyperpolarization Abbreviations: Ach, acetylcholine; CAP, compound action potential; DP, distortion product; EOAE, evoked otoacoustic emission; GABA, was increased by an application of benzodiazepines Q-aminobutyric acid; IC, inferior colliculus; LOC, lateral olivococh- (Plinkert et al., 1993). GABA also decreased the electro- zlear; MOC, medial olivocochlear; OAE, otoacoustic emission; SL, motile response (Sziklai et al., 1996). In contrast, Evans sensation level; SPL, sound pressure level; SOAE, spontaneous otoacoustic emission; SOC, superior olivary complex et al. (1996) observed no OHC response during whole- 0378-5955 / 98 / $19.00 ß 1998 Elsevier Science B.V. All rights reserved. PII: S0378-5955(98)00068-9 HEARES 3034 29-6-98 72 N. Morand et al. / Hearing Research 121 (1998) 71^76 cell recording after GABA application. In vivo, OHC GABA is an inhibitory transmitter which is abun- function can be explored by otoacoustic emission dant in the central auditory pathways (Wynne et al., (OAE) recordings. OAEs are sounds recorded in the 1995; Vater et al., 1992; Fubara et al., 1996). It has external ear canal in the presence of acoustic stimula- been shown that benzodiazepines increase the CAP and tion (evoked OAEs (EOAEs) and distortion products decrease cochlear microphonics in guinea pigs, in con- (DP)) or without acoustic stimulation (spontaneous trast to electrical stimulation of the crossed olivo- emissions (SOAEs)). OAEs are generated in the coch- cochlear bundle. These benzodiazepine e¡ects have lea, probably by OHC motile activity. The in£uence of been thought to re£ect a central action of GABA on benzodiazepines on EOAE amplitude has been studied the e¡erent system (Velluti and Pedemonte, 1986). in humans: Hauser et al. (1992) found no signi¢cant Thus GABA may have a peripheral action on outer di¡erence in EOAE amplitude under premedication hair cell mechanisms, and a central action on the medial with midazolam; likewise diazepam and £unitrazepam e¡erent system. The aim of the present study was to had no e¡ect on EOAE amplitude (Delb et al., 1994). It investigate these two hypotheses in humans by studying has been shown that contralateral acoustic stimulation benzodiazepines known to produce their pharmacolog- decreases the EOAE amplitude in humans (Collet et al., ical e¡ect by interacting with GABAergic inhibitory 1990) and acoustic DPs in guinea pig (Puel and Rebil- neurotransmission and their e¡ect on EOAE amplitude lard, 1990). The medial e¡erent system is involved in and on the MOC system, by comparing EOAE ampli- this contralateral suppression e¡ect, which is greatly tude with and without contralateral acoustic stimula- reduced in humans after sectioning of the vestibular tion (Collet et al., 1990; Veuillet et al., 1991). nerve, which severs olivocochlear e¡erents (Giraud et al., 1995). Thus this suppression e¡ect observed on EOAEs in the presence of contralateral acoustic stim- 2. Methods ulation is a good means of investigating the MOC sys- tem in vivo. In guinea pigs, the perfusion of the cochlea 2.1. Subjects with bicuculline (GABA antagonist) abolished the f23f1 DP reduction normally observed after contralateral The study was performed on 10 healthy men ranging stimulation in guinea pigs (Kirk and Johnstone, 1993), in age from 20 to 34 years (mean 24 years, S.E. 1.23). thus con¢rming a role for GABA in the OHC mecha- All the subjects were volunteers and this study was nism. So the terminal elements involved in the contra- carried out with their written consent and with the lateral acoustical suppression of f23f1 can be identi¢ed agreement of the local institutional Ethics Committee. as being part of a GABAergic innervation, whether The subjects were selected according to the following LOC or MOC system, of the apical OHCs. acoustic criteria: normal auditory thresholds ( 6 20 dB Thus a majority of studies con¢rm the presence of loss between 250 and 8000 Hz by octave) measured by a GABAergic e¡erents on OHCs and presence of Madsen DAIII audiometer, normal tympanometric re- GABAA receptors on the basal pole of OHC, but there cordings done using an Amplaid 702, presence of is no evidence of a real action of GABA on outer hair EOAEs (amplitude better than 5 dB SPL at 80 þ 3 dB cell mechanisms. Furthermore the presence of GA- SPL), no spontaneous otoacoustic emissions. The vol- BAergic synapses in human cochlea has not been unteers were all right-handed (Ol¢eld, 1971). studied. A questionnaire and a medical examination further On the other hand, the olivocochlear e¡erent system enabled selection of subjects without prior acoustic could be under the control of central auditory path- pathology, taking no medical treatment, using no hyp- ways. The inferior colliculus (IC) receives descending notics or benzodiazepines. On the day of experimenta- input from the auditory cortex, and sends ipsilateral tion a urine assay for benzodiazepine was made to con- and contralateral projections onto the medial olivo- ¢rm the last of these conditions. cochlear system (Hu¡man and Henson, 1990). So it is anatomically possible that the IC plays a role in the 2.2. Otoacoustic emissions activity of the olivocochlear e¡erent system. Further- more, physiological studies show an IC contribution EOAE recordings were made with subjects reclining to the olivocochlear e¡erent system. Stimulating the in a sound-proof room, using an Otodynamics0 ILO IC induces a decrease in compound action potential 88 apparatus. A probe placed in the external ear canal (CAP) (Dolan and Nuttal, 1988a) that is similar to delivered acoustic stimulation through a loudspeaker the change seen after electrical stimulation of the (Knowles 1712 transducer) and recorded responses crossed olivocochlear bundle (Dolan and Nuttal, with a microphone (Knowles 1843). To be sure that 1988b). Furthermore, stimulating the IC protects the the probe was always placed in the same position cochlea from noise, as does stimulation of the crossed over successive recordings, a silicone mold of the probe olivocochlear bundle (Rajan, 1990). and of the external ear canal was made. HEARES 3034 29-6-98 N. Morand et al. / Hearing Research 121 (1998) 71^76 73 Stimuli were non-¢ltered clicks with a duration of 80 Ws and a rate of 50/s. Linear and non-linear di¡er- ential cochlear echo methods were used (Kemp et al., 1990). 2.3. Procedure During this study a double-blind administration of oxazepam versus placebo was made (the kind of molec- ular administered was not known either to subjects or to experimenters). So the data were collected in a blinded manner. The subjects were tested before and 1, 3, 7 and 24 h after oxazepam (20 mg) or placebo administration. The order of testing (oxazepam versus placebo) was randomized. We employed a crossover design: all 10 subjects were tested twice with a 2-week interval (once after oxazepam intake, and once after placebo intake). EOAEs were recorded in right ears. Fig. 1. Mean plasma concentration 1, 3, 7 and 24 h after oxazepam A ¢rst recording was made with a non-linear click at intake.
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