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VariabiliW of the influence of a visual task on the active micromechanical propert of the cochlea Patrick Froehlich 1, Lionel Collet 1'2, Jean-Marc Chanal 1 and Alain Morgon ~ l Laboratoire d'Explorations Fonctionnelles Neurosensorielles, H6pital Edouard Herriot, Lyons (France) and 2Laboratoire de Physiologie Sensorielle, Facult~ de M~decine Lyon-Sud, Pierre-B~nite (France)

(Accepted 17 October 1989) Key words: Attention; Evoked otoacoustic emission; Olivocochlear; Efferent; Visual

The effect of a visual task on the active micromechanical properties of the cochlea studied by the evoked otoacoustic emissions (EOAEs) has been the subject of only one published study (Brain Research, 44 (1988) 380-383). In order to examine the reliability of this effect, a similar study has been run on 16 subjects. A significant decrease in EOAEs during a visual task was obtained for 3 subjects. The two subjects whose decrease was the most significant were tested again one month later and the same effect was found. This striking interindividual variability is discussed in terms of olivo-cochlear neuronal excitability. The olivocochlear efferent system initially described by Rasmussen 16 is composed of two subsystems: the medial system which continues to the outer hair cells (OHCs) of the organ of Corti, and the lateral system which continues to the dendrites of the afferent cochlear neurons near the inner hair cells (IHCs) 18. The effect of selective attention on peripheral auditory transmission as indexed by brainstem auditory evoked potentials (BEAP) has been the subject of several studies and an ongoing controversy. Some have shown an effect of attention on BAEPs 2'1°, whereas the others could not confirm such an effect 3A3'14. BAEPs more specifically reflect the activity at the level of the afferent cochlear neurons, which essentially make synapses with the inner hair cells (IHCs) and not with the outer hair cells (OHCs) of the organ of Corti. In addition, from a technical point of view, it is necessary to use stimulus intensities higher than or equal to 40 dB hearing levels (HL), and a great number of sweeps is necessary to reduce the variability of the measures of the amplitude. Therefore, the duration of the attention task is increased 4. E O A E s which are sound-emitted by the cochlea in response to an auditory stimulation 7 constitute another way to study the peripheral effect of attention. They reflect the contractile activity of the OHCs of the organ of Corti, which are richly innerved by the medial efferent system. The excitation of this system by means of a contralateral auditory stimulation decreases the amplitude of the E O A E s 6. The E O A E s can be reliably

obtained in response to auditory stimulation of low and even subliminal intensities 5. Their recording requires a low number of sweeps compared with the BAEPs. Only one study has been published on the role of attention (by means of a visual task) on the EOAEs. It reported a decrease of the intensity of the highest frequency peak of the spectral analysis of the E O A E s 11. This decrease persisted during the 5 min of the attention task. Because of the importance of this result and of the controversy existing on the effect of attention on the BAEPs, the purpose of our work was to try to find this effect using a brief visual attention task (identical to the one previously used by Lukas 9. Sixteen volunteers (7 men and 9 women) between 13 and 38 years old (mean = 24.44 years; S.D. = 8.29 years) without auditory or visual loss were tested. The recording of the E O A E s was carried out in response to non-filtered clicks of 80/~s by means of the method proposed by Bray and Kemp 1. The probe was composed of a Knowles 1843 emitter and a BP 1712 microphone embedded in a plastic ear plug. The E O A E s were analysed during the 20 ms after the stimulus, averaged over 512 responses, and filtered with a pass-band of 500-6000 Hz. Stimulus presentation, data recording, averaging, and spectral analysis were carried out with the ILO 88 of Otodynamics. The intensity of the auditory stimulus in the external ear canal was measured by the ILO 88 and was adjusted to produce an intensity of 63 dB sound pressure level (SPL) (_+ 3 dB). The procedure consisted of

Correspondence: L. Collet, Laboratoire d'Explorations Fonctionnelles NeurosensorieUes, H6pital Edouard Herriot, Pavilion U, 3 place d'Arsonval, F-69003 Lyons, France.

0006-8993/90/$03.50 ~) 1990 Elsevier Science Publishers B.V. (Biomedical Division)

287 r e p e a t i n g 4 recording conditions 5 times each in r a n d o m order: (1) recording of the E O A E s without visual task and without contralateral auditory stimulation; (2) recording with a visual task consisting of the r a n d o m p r e s e n t a t i o n on a television screen of two letters ( O and Q) at a frequency of 2/s. The subjects counted mentally the target letter Q and r e p o r t e d at the end of the trial the n u m b e r they had o b t a i n e d . The c o m p u t e r p r o g r a m , by giving at the end of the test the n u m b e r of Qs, allowed us to control the exact counting by the subjects. No m o t o r task was asked in o r d e r to eliminate any effect due to m o t o r origins; (3) recording during a contralateral auditory stimulation by a b r o a d band white noise of 50 dB SPL; (4) concurrent presentation of the previous visual task and the contralateral auditory stimulation. T h e p a r a m e t e r studied was E O A E amplitude measured in dB SPL over the entire 20 ms sample time (i.e. equivalent p o w e r continuous level). The results based on the average of the intensity of the E O A E s in each test condition show a significant difference according to the condition of recording: m e a n (control) = 8.31 dB; mean visual attention = 8.29, m e a n (white noise) = 7.56 dB: m e a n (white noise + visual attention) = 7.63, residual s t a n d a r d deviation = 0.337, 47 df, F3•4s = 23.42, P < 0.0001 ( A N O V A with r e p e a t e d measure (Fig. 1). This significant overall F ratio was due to the effect of contralateral auditory stimulation by white noise (in c o m p a r i s o n to control t -- 6.26, 45 df, P < 0.001) and not to the effect of the visual task (in comparison to control t = 0.126, 45 df, N.S.) Nevertheless in 3 out of the 6 subjects, there was a significant decrease of the amplitude of E O A E s during the visual task ( M a n n - W h i t n e y U-test: P < 0.01 for 2 subjects and P < 0.03 for the third one). Four weeks after this recording, the two subjects whose decrease was the most significant were tested again according to a procedure identical to the previous one, in o r d e r to verify the replicability of the effect of attention on E O A E s . The

first subject (male, 23 years old) showed a decreased intensity of E O A E s over 9 consecutive runs c o m p a r e d to the control condition (m -- - 0 . 1 9 dB). The second subject (female, 29 years old) showed a decrease in the intensity of E O A E s during the visual task over 7 consecutive runs (m = - 0 . 3 7 dB) (Fig. 2). These two results were statistically significant ( M a n n - W h i t n e y Utest: respectively P < 0.05 and P < 0.0001). Two arguments allow us to rule out a possible role of the middle ear as a factor in these results. First of all, the spectral analysis of E O A E s by frequency bands (0-1000 Hz, 1000-2000 Hz, 2000-4000 Hz) with and without the attention task, showed that the effect of visual did not b e a r on the frequencies of E O A E s lower than 1000 Hz s. On the other hand, there was a significant decrease in the intensity of E O A E s for both subjects for the 1000-2000 Hz band (respectively, U -- 0, P < 0.001 and U = 11, P < 0.05) and the 2000-4000 Hz b a n d for the first subject (U = 16, P < 0.05). F u r t h e r m o r e , a variation of pressure in the middle ear only slightly modifies the intensity of E O A E s for low frequencies and a substantial pressure is required to p r o d u c e an effect 8. The second argument is that for these two subjects, the measure of impedance in the middle ear was carried out in the presence and absence of the visual task 5 times in a row and did not show any modification. These results show, at least for two subjects, a reproducible intrasession and intersession effect of attention on E O A E s , which must be related to a modification

Relative EOAE Amplitude (dB) 0.2

O Subject 2 (n=7)

0.0 -0.2

• Subject 1 (n:9)








-0.6 -0.8 -1 Fig. 1. Evoked otoacoustic emissions and spectral analysis of one subject under attend (A) and non-attend condition (C). Each raw data is the average of 512 responses. (Time period is 20 ms.) Each OAE is the average of two independent measurements (A and B). The spectral analysis shows the real response in outlined plots and the random noise (A-B) in solid plots. Echo is the intensity of this average, A-B shows the intensity of the noise (obtained by subtracting the two responses A and B). Repro is the value of the cross-correlation between A and B.






Fig. 2. Effect of visual attentional task (A), simultaneous contralateral white noise (WN) and of the combination of attention with white noise on the intensity of EOAEs. The intensity from the control condition (C) is expressed as a reference value equal to 0 dB. For each subject intensity of EOAEs decreases significantly during the attentional task.

288 of the active contractions of the O H C s of the organ of Corti u n d e r the action of the medial efferent system. It has been shown on animals that an electrical stimulation of this system can modify the cochlear micromechanical responses 1°'16. It seems that there exists an efferent neuronal control of the active cochlear micromechanical properties. This study did not find as many subjects presenting an effect of attention as in Puel's study 14 (3 of 16 against 13 of 16 subjects). The explanation for this discrepancy could be based, in our view, on technical differences. The studied p a r a m e t e r was not the same: in their study Puel et al. m e a s u r e d the variation of the a m p l i t u d e of the d o m i n a n t frequency emitted, where in our study it was the E O A E amplitude m e a s u r e d over the whole sample time. H o w e v e r , in our study the analysis of the a m p l i t u d e of the d o m i n a n t frequency did not improve our results. But the analysis times were 30 ms for Puel et al. and 20 ms for us. This reduction leads necessarily to wider bandwidths, as shown by spectral analysis. O n e can suggest that the effect of attention may vary according to the spectral c o m p o n e n t s . F u r t h e r m o r e , in animal studies, the efferent system shows a substantial interanimal variability9. I n t e r s u b j e c t differences in the excitability of

the efferent system could thus explain differences of the effect of attention task from one subject to another. The result, that we noted, is linked to the visual task. But the p r o c e d u r e d o e s n ' t allow us to confirm if it is due to an effect of selective attention. It could be simply a non specific result d e t e r m i n e d by the subject's general arousal and alertness levels lz. The effect of selective attention can be d e m o n s t r a t e d only in experiments where two or more channels of stimuli are present in the environment and when attention is switched from one to the other. While a large effect of contralateral white noise on the E O A E s was found in a g r e e m e n t with previous work 6, the combination of visual task with white noise did not show any difference with respect to white noise alone. F u r t h e r studies using an efficient selective attention p r o c e d u r e on a greater n u m b e r of subjects are necessary before a conclusion can be given on the effect of the selective attention and of the association of attention with white noise.

1 Bray, P. and Kemp, D.T., An advanced cochlear echo technique suitable for infant screening, Br. J. Audiol., 21 (1987) 191-204. 2 Brix, R., The influence of attention on the auditory brain stem evoked responses, Acta Otolaryngol., 98 (1984) 89-92. 3 Collet, L. and Duclaux, R., Auditory brainstem evoked responses and attention, Acta Otolaryngol., 101 (1986) 439-441. 4 Collet, L., Hellal, H., Chanal, J.M. and Morgon, A., Are BAEP and MLR suited for the study of a hypothetical peripheral selective attention effect?, Int. J. Neurosci,, 41 (1988) 97-102. 5 Collet, L., Les oto~missions, Les Nouveaux Cahiers de la CFA, Paris, 1988, 59 pp. 6 Collet, L., Kemp, D.T., Veuillet, E., Duclaux, R., Moulin, A. and Morgon, A., Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects, Hearing Res., in press. 7 Kemp, D.T., Stimulated acoustic emissions from the human auditory system, J. Acoust. Soc. Am., 64 (1978) 1386-1391. 8 Kemp, D.T., Ryan, S. and Bray, P., A guide to the effective use of otoacoustic emissions, Ear Hearing, in press. 9 Liberman, M.C., Physiology of cochlear efferent and afferent neurons: direct comparisons in the same animal, Hearing Res., 34 (1988) 179-192. 10 Lukas, J.H., Human auditory attention: the olivocochlear bundle may function as a peripheral filter, Psychophysiology, 17 (1980) 444-452.

11 Moutain, D.C., Changes of endolymphatic potentials and crossed olivocochlear bundle stimulation alter cochlear mechanics, Science, 210 (1980) 71-72. 12 Naatanen, R., Selective attention and evoked potentials in humans - - a critical review, Biol. PsychoL, 2 (1975) 237-307. 13 Picton, T.W. and Hillyard, S.A., Human auditory evoked potentials II: effects of attention, E.E.G., Clin. Neurophysiol.. 36 (1974) 191-199. 14 Picton, T.W., Stapels, D.R., and Campell, K.B., Auditory evoked potentials from the human cochlea and brainstem, J. Otolaryng., 10 (1981) 1-41. 15 Puel, J.L., Bonfils, P. and Pujol, R., Selective attention modifies the active micromechanical properties of the cochlea, Brain Research, 44 (1988) 380-383. 16 Rasmussen, G.L., The olivary peduncle and other fiber projections of the superior olivary complex, J. Clin. NeuroL, 84 (1946) 141-218. 17 Siegel, J.H. and Kim, D.O., Efferent neuronal control of cochlear mechanics? Olivocochlear bundle stimulations affects cochlear biomechanical non linearity, Hearing Res., 6 (1982) 171-182. 18 Warr, W.B, and Guinan, J.J., Efferent innervation of the organ of Corti: two separate systems, Brain Research, 173 (I979) 152-155.

The authors wish to thank Mrs. A. Vidal for editing the manuscript.

Variability of the influence of a visual task on the active micromechanical properties of the cochlea.

The effect of a visual task on the active micromechanical properties of the cochlea studied by the evoked otoacoustic emissions (EOAEs) has been the s...
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