Sectioning the efferent bundle decreases cochlear frequency selectivity

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(Received~May2~th;/1981 ;iRevised version :re,~ived and accepted October 28th, 1981)

Key,words: !cochlea,-efferent bun~fle - frequency selectivity

Cochlear frequency selectivity wa~ tested ha, ra'~ and eats before and after sectioning the vestibular nervewhichearries the efferent bm~dle to the, eechlea. Compound action potemia~ tuning curve were obtain~l by a s~ultaneous masking procedure:: Transection of the efferent bundle resulted: in all group of animals, i n an enlargement of tip segment o f the tuning curve. T h e Q~0 dB value decreased by abO"t 30¢/o wi~hout,~y"sigl~c~ult threshold cha~e. T h ~ $ e r e s u l t s ~ k e n together with previous developmental findings, suggests t h a t efferentsrto ouler hair cells could piay a role in sharpening the frequency selectivity of the cochlea. ~

How the cochlea achieves frequency sJec~wlty, 1.c. the ability to separate iudividual components of a complex signal,, remains one of the major problem !n peripheral acoustic physiology. Thus, it iis difficult to explain the difference~ between :the broad mechanical tuning of the basilar membrane [l, 30] and the sharp tuning of the single auditory nerve fiber [8:, 16], the spiral ganglion neurov, s ~25], ana, the, inner 'hair cells ([HC)' [26]. Recently, some authors have claimed that the basilar membrane couldbeas Sharply tuned as the fibers [! 7, 24]. Meanwhile, most of them-espouse a sharpening mectmnism phyed bya ,second filter', and ~:herote o ¢ outer hair cells (OHC)in such ~a pr~>:ess has been put forward (see ref. 9). Some investigators haveMso examined the activity of the efferent ~ystem, whic!,~predominantly innervates :OHC. To date, the physiological and, therefore, the behav'~oral roles of the efferentsystem to the cochlea remains a puzzling question. Ir~ fact most of the available data: are based ulx~n electrical stimulation of the crossed o]ivocochlear bundle (COCB), which is far from a pure physiolo#cat condition. They showmainly an inhibitory effect on the acoustic input ~6, t3], with an k~crease in the cochlear microphonic potential ~10]. Among the propozed actions of the efferent ~

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system on auditory perceptu~A proc~ses (see ref. 18), some invesfig,Ltors have reported a possible action on frequency encoding. Such resu|ts have to be carefully considered as they do not all agree. For instance, COCB stimulation was shown to reduce the sharpness of tuning:0f singie auditory nerve fibres:j29| ~l~d :~o:!ialter:or enhance th~ nm~kLng effect depending on the click :-Mtensity [22], :In b e h ~ 0 r ~ studies, transection of the same bundle altered discrimh'iative cochlear ab~ifieSi~::in monkeys ~2, 7, 27] but not in cats [15]. ~ Our work on the development of cochlear ~tructure axM function: proVidedan indication o f a: possible action of O H C efferems i n frequency::~ selecfivky mechanisms. Indeed, a very close time relationship was found ~tween the latest stage of OHC deveiopment, ~which is ~ e formation of large e:fferent:synapses at their base [23], and the sharpening of cochlear action potential tuning curves (APTC) [4]. Was this only a coincidence, or are the two phenomena really related? To answer this question, we chose to compar the tuning of ATPC, as expressed by the Q~0 value, before and after sectioning the vestibular nerve which carries the efferent bundle to the cochlea. All operated animals (23 rats and 3 cats) were anesthetized with sodium pentobarbim| (40 mg/kg, i.p.). The vestibular nerve:was ~sec6oned near:the brainstem at the internal auditory meatus through a ~'anscerebellar approach. Hearing tests were performed on 4 groups of animals: groUp:I, normal ra~s ( n = 17); group I], rats (n = 13) tested one month after the surgery; group Ill, rats (n = 10) ~es~ed during surgery just before and just after sectioning the vestibular nerve; and group IV, ca~s {n = 3) tested before and one momh after surgery, in all groups, the hearing l~s~ were performed by recording, under light anesthesia, ~he gross action potential a~ ~he round window. Initially, an audiogram was made by determining ~hreshohs for frequencies ranging between 0,5 ~nd 20 kHz, Animals wi~ a threshotc elevation more than 15 dB above ~he normal values for rais or ca~s, were sysiemati~ally rejecied. In the remaininganima|s, the frequency se|ectivi~y was then determined at different test frequencies using A P T C m e t h o d r with sims. ,aneous m~z~sking [5]. The sharpness Of tuning curves was indica~edby measuring iheQi0 value, which is ,he ratio of the characteristic frequency to the 10 dB: bandwidth above ~hreshold. Auditory stimulations by tone burst were made in fr~,field, ic~side a sound-proof and anechoic room, After iesting, cochleas were fL~ed~removed and prepared classically [12] for electron mzcroscopy. S u b s e q u e nMstolog~cal t" " mves~l" " ga~ions were done using serial semi.thin sections (10-20/~m), toensure the absence of efferent fibers crossing ,he ,unne] of Corti, and ~o confirm ~he disappearance of efferent endings at OHC level. APTC recorded in all groups showed some constant and characteristic features (Fig. I). The overallshape ofthecurves fitted classical descrlpt~ ~s~ witha sharp tip segment centered on ~es, frequency, a s~rong cut,off fo~ f~iquencies above test frequency, and an elongated low-frequency: ~il,.Af~er:,ect~omng theefferen~ bundle (Fig. 1, do~ed curves), whi~e auditory threshold did not change, modificartion~ of "

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Fig. 1, Samples of action potential tuning curves (APTC) before (open circles) and after (filled circles) sectioning the efferent bundle. APTC were obtainLed by the simultaneous masking procedure. Each circle represents, for each masker frequency, |he intensity able to suppress the test frequency set l0 dB above threshold (in brackets). The Qm value indicating the sharpness of the tip segment is expressed on the upper right of the curves. A: rat, APTC at tesl frequency 10 kHz obtained during ,:,urgery, just before and after transection of the vestibular nerve. Note, after transection (dotted line) the Q~0 decrease and the elevation of the lowest point of the tip. B: cat, APTC at test frequency 4 kHz obtained before and one

month after surgery. Sectioning the efferent system has resulted (dinted line) in a -~rong Q~0 decrease, while the lowest point did not really change and llhe low-frequency tail was lowered

APTC :were noted. !n some cases an e~evation of the lowest poin~ of the tip was noted (Fig.:lA), others showed a lowering of the low-frequency tail~ (Fig. 1B). But in all cases, an obvious widening of the tip segment appeared. Measares of the Qlo values taken from the 3 groups of rats are displayed in Fig. 2. In nc~rmal adult rats group (I) values are indicated for 3 test frequencies (6, 8 and 10 kHz), and range between 2 and I L By comparison, ;for rats one month after vestibular surgery (gr,~UP H), .thesevalues ranged from I to 7 (Fig. 2A). The mean Q~3 were decreased in i:O~mt~anima~sby30-40% (Fig. 2B). Group H1, i.e. rats tested during surgery jus~::before and after sectioning, of the efferent dunbIe, sL,ewed siv~ilar variations (Fig. 2C,: D)- for differenttest frequencies (6, 8, 10and 15 ~Hz), a decrease ir~ mean

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dig..k Ql0 values of APTC bel ore ~[opeacircles) apt: after (filled circles) s~tioning ~.heefferent system. A: Qa0 distribution in normal rats (n = 17) and one .~.....lth after surgery (n = 13) at 3 t.:st frequencies (6, 8

and iG kHz). B: mean Qm for the :samegroups of ra~s, with SEM. C: Qio distribution in rats (n .:, 10) ~ested during surgery just before and after sectioning the vestibular nerve, at 4 test frequencies (6, 8, 10 .and 15 kHz). D: mean Q0o for the same t;roup, with S.E.M. In A and C Qlo with or without efferents are sigrfi,qcamly different at P < 0.05. Sectioning the efferent system r,'gulted in lowering mean Qlo by 20-*)%.

Ql0 values was observed ranging between 20 and 40%. Similarly, in cats after sectioning the efferent bundle (group IV), the Qlo decreased by 2 0 - 5 0 % . Before interpreting the above results one must remember that APTC were recorded with a simultaneous masking procedure, not with forward masking. This means that a widening o f the tip segment does not necessarily a change in tuning, but a change in tuning and/or a second phenomenon which is likely related to two-tone inhibition or interference [19]. We now can focus on the two main consequences of cutting the efferent bundle, as showr~ by our results, First, a threshold. This observation is supported by:ex~rimental: data [7,-::-ilS]i~and~:dini~l observation in patten ts with Meniere's disease fin WhiCh:~th~ ves~ibhlarl,nervehas~ ~ e nL:* cut it4], Second, APTC recorded from c ~ h l e a s without efferent supply .~how:a

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30~o; ricerease)ha shar~nhagi .as ~'e×pressed by the Qlo value. Thus.,-the efferent system could play a role ha increashag the cochlear frequency selectivity. A question arises!fromthis:c6ne~uSion: which 0neofthe two separate efferent systems recently prolmsed [28] could be involved? In tlhis experiment both efferent systems were cut. BU!.it ~msdfffieult:toattribute a~rol~infrequency selectivity to the efferent system m~i~y!!~eonn~t~il to>itHC:.-:-.Aetually;during development this part of the efferent

s ~ t ~ ma!ure!i@eryear!y[3; 123], far before any cochlear frequency selectivity can if any, must then be related to How can Suchla:rolebeexplained? One has to envisage here the overall function of OHC: T~iey:aresupposed toplay an ~ndkeet role on the sensory message mainly issued from IHC [26].: It has been proposed that OHC play this indirect role through a mechame~ e0~phng of their stereoctha w~th the rectorial membrane [12]. Another proposal is that of an OHC:modulafion of the IHC electrical environment [20]. In both cases the efferent system going to OHC could be involved, since stimulation of COCB acts on the endocochlear potential [l 1], as well as on cochlear mechanics [21]. This work was supported by grants from I.N.S.E.R.M. (ATP 79-It3) a~d C.N.R,$. (RCP 537). We thank Dr. G,,R. Book and Dr. M.C. Remond for critically reading the manuscript. 1 Bekesy, V.G., Ober die mechanische fr~quemmnzlysein der schnecke ve~'schiedenert/ere, Akust. Z., 9 (1944) 3-11. 2 Capps, M.S. and Ades, H.W., Auditory frequency discrimi~=ationafter transection of the olivocochlear bundle in squirrel monkeys, F×p Neurol., 21 (1968) t47-158. 3 Carlier, E. and Pujol, R., Early effects of efferent stimulation on the kitten cochlea, Neurosci. Lett., 3 (1976) 21-27. 4 Carlier, E., Lenoir, M. and Pujol, R., Development of cochlea frequency selectivity tested by compound action potential tuning curves, Itear. Res., 1 (1979) 197-201. 5 Dallos, P. and Cheatham, M.A., Cow pouad action potential (AP) tuning curves, J. Acoust. S~:. Amer. 59 (1976) 591-597. 6 Desmedt, J.E., Auditory evoked potertials from cochlea to cortex as influenced by activation of efferent olivo-cochlear bundle, J. Acoust. Soc. Amer., 34 (1962) 1478-149(. 7 Dewson, J.H., Efferent olivocoeblear bundle: some relationships to stimulus discrinfination in noise, J. Neurophysiol., 31 (1968) 122-130. 8 Evans, E.F., The frequency response and other properties of single fibre in the guinea pig cochlear nerve, 3. Physiol. (Lond.), 226 (1972) 263-287. 9 Evans, E.E, The sharpening of c~hlear fi'equency selectiw:ty in the normH and abnormal cochlea, Audiology, 14 (t975) 419-442. 10 Fex, J., Augmentation of cochlear microph~n~c.~by stimulation of efferent fibres to the cochlea, Ac~a otolaryng., 50 (1959) 540-541. 11 Fex, J., Efferent inhibition inthe cochlea by the olivocochlear bundle. In A.V.S. de geuck and " Kmght ~ s . ) , Heating Mechani~a in Vertebrates, Churchill, London, 1968~ pp. 169- ~8t. 12 Flock, A.P,I and Cheung, H., Action fflame~tts in sensory hairs of the inner ear, J. Cell Biol., "5 (1977) 339-343.

13 G~ambos, R., Suppressionof avdito~~ne~e ~.c~vity by s~mu~tionof.effercm, fibres.i~to.¢och|ea~iJ~

NeuroMgical Aspects of Auditory and Vestibu|ar I~sorders, Thomas, rspi~ngfie~d~ IL, l ~ ! ! p p . 94-103, 15 igarashi, :J.L,~ Nak~i,~¥. a n d Mford. B,R,: Mavioml iaudito~,: funcfioa iaftcr~ transectionof crossed o l i v ~ k a r IVandl natiorh Acmotolaryng,, 87 (1979):7~83, 16 K~ang, N.Y.S., Watanabe, T., Th0mas, E.C~ and Clark, IL.F,, Di~harg¢ tmRemsof singlefibrcsin I

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17 Kim, D.O., Molnard, C.E. arm Pfeiffer, R.R., A sys,iemof:n~lin~i'::!diffdi~ntia!ilequafioml" modelling basilar membrane motion. J. Acoust. Soc. Amer., 54 (1973)151%i529;/ : ~ :: •~' 18 Klinke, R. and Galley, N,, Efferent innetvafion of vestibular andaudit0rY rec~tors, PhYsioLRoy.' 54 (1974) 316-357. : 19 Legouix, J.P., Remond, M.C. and Gre~nbaum, H., Interference and two-toneinhi~ition, J, Acous~i Soc. Amer.. 53(1973) 409-419. 20 Manley, G., Cochlear frequency sharpening - a new synthesis, Acta oto!aryng, 8.~ (1978)I,167-176. 21 Mountain. D.C,, Changes in endolymphatic potential and crossed olivo-cochlear ~undle stimulation alter cochlear mechanics, Science, 2 lO (I980) 71-72, 22 Nieder, P. and Nieder, I., .Mltimasking effect of crossed olivo-cochlear bundle stimulation with loud clicks in guinea pig, Exp. Neurol., 28 ( 1 ~ 0 ) r 179-188. 23 Pujol, R., Carlier, E. and L'~vigne, C., Different pattern of cochlear innervadon during the d,:vel0pment of the kitten, J. comp. Neurol., 177 (~978) ~29-:535. 24 Rhode, W.S., Some observations on cochl~tr mechanics, J. Acoust. Sac, Amer;66.(19"/8)158--176. 25 Robertson, D. and Manley, G.A., Manipulation of frequency Analysis in the cochlearganglion of the guinea pig, J. comp. Fhysiol., 91 (i974) 363-37[;. 26 Russel, I.S. and Se~lick, P.M., lntracellular studies of hair cells in the n ammalian cochlea, J. Physiol. (Lond.), 224 (1978) 261-290. 27 Trahiotis, C. and Elliott, D.M., Behavioral inve~tigation of some po, sible effects of sectioning the crossed olivocochlear bun~le, J. Acoust. Soc. Amer., 2 (197,)) 592-596. 28 Warr, W.B. and Guinan, I.J., Efferent Jnnervation of the organ of Corti: two separate systems, Brain Res., 173 (1979) 152-155, 29 Wiederhold, M.L.. Variatiom in the effects of electric stimulations of the crossed o!ivo-cochlear bundle on cat single auditory nerve-fiber-responses to tone burst, J. AcousL Soc. Amer:, 48 (1970) 966-967. 30 Wilson, J.P. and Johnstone, LR., Basilar membrane and middle.ear vibration in guinea pig measured by capacitive probe, .L Acoust. Soc. Amer., 55 (1975) 606-521. .

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