Cerebral Cortex Advance Access originally published online on September 8, 2005
Cerebral Cortex 2006 16(7):941-948; doi:10.1093/cercor/bhj035
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Evidence for Corticofugal Modulation of Peripheral Auditory Activity in Humans
1 Service d'Audiologie et Explorations Orofaciales, Centre Hospitalier Lyon-Sud, 165 chemin du Grand Revoyet, 69495 Pierre-Bénite cedex, France, 2 Laboratoire ‘Neurosciences & Systèmes Sensoriels’, CNRS UMR 5020, Université Claude Bernard Lyon 1, 50 avenue Tony Garnier, 69007 Lyon, France, 3 Service de Neurologie Fonctionnelle et d'Épileptologie, Hôpital Neurologique et Neurochirurgical, 59 boulevard Pinel, 69677 Bron cedex, France, 4 Service de Neurochirurgie Fonctionnelle (Pr M. Sindou), Hôpital Neurologique et Neurochirurgical, 59 boulevard Pinel, 69677 Bron cedex, France and 5 Institut Fédératif des Neurosciences de Lyon, IFR 19, Bâtiment B13, Hôpital Neurologique et Neurochirurgical, 59 boulevard Pinel, 69677 Bron cedex, France
Address correspondence to Xavier Perrot, Service d'Audiologie et Explorations Orofaciales, Pavillon 3A, Centre Hospitalier Lyon-Sud, 165 chemin du Grand Revoyet, F-69495 Pierre-Bénite cedex, France. Email: xavier.perrot{at}chu-lyon.fr.
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Abstract |
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Active cochlear micromechanisms, involved in auditory sensitivity, are modulated by the medial olivocochlear efferent system, which projects directly onto the organ of Corti. Both processes can be assessed non-invasively by means of evoked otoacoustic emissions. Animal experiments have revealed top-down control from the auditory cortex to peripheral auditory receptor, supported by anatomical descriptions of descending auditory pathways from auditory areas to the medial olivocochlear efferent system and organ of Corti. Through recording of evoked otoacoustic emissions during presurgical functional brain mapping for refractory epilepsy, we showed that corticofugal modulation of peripheral auditory activity also exists in humans. In 10 epileptic patients, electrical stimulation of the contralateral auditory cortex led to a significant decrease in evoked otoacoustic emission amplitude, whereas no change occurred under stimulation of non-auditory contralateral areas. These findings provide evidence of a cortico-olivocochlear pathway, originating in the auditory cortex and modulating contralateral active cochlear micromechanisms via the medial olivocochlear efferent system, in humans.
Key Words: active cochlear micromechanisms • efferent auditory pathways • evoked otoacoustic emissions • intra-cerebral electrical stimulation • refractory epilepsy
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Introduction |
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Neuroanatomical and histological studies in animals, including non-human primates, have disclosed corticofugal descending auditory pathways linking the auditory cortex to the cochlea via the medial olivocochlear efferent system (MOCES) (Huffman and Henson, 1990
; Mulders and Robertson, 2000a; Doucet et al., 2003). The medial olivocochlear bundle (MOCB), originating in the vicinity of the medial nuclei of the brainstem's superior olivary complex, predominantly projects onto the contralateral cochlea, where it synapses with outer hair cells (OHCs) (Warr, 1992). OHCs, by virtue of their somatic electromotile property (Zheng et al., 2000), are thought to constitute the anatomical substrate of active cochlear micromechanisms (ACMs), thereby accounting for the exquisite auditory sensitivity and fine frequency selectivity of the normal ear (Siegel and Kim, 1982; Brownell et al., 1985). In addition, electrophysiological studies have highlighted multiparametric corticofugal influence on both the subcortical auditory nuclei and the organ of Corti in sound processing such as frequency, amplitude, duration or spatial tuning (Huffman and Henson, 1990; Torterolo et al., 1998; Mulders and Robertson, 2000a; Suga and Ma, 2003). Taken together, these findings suggest that the descending auditory pathways mediate a functional feedback loop which enables the auditory cortex, via the MOCES and a modulation of OHC electromotility, to adjust afferent signals from the earliest stages of peripheral auditory processing (Huffman and Henson, 1990; Mulders and Robertson, 2000a; Xiao and Suga, 2002a,b).
In humans, only the most distal part of the descending auditory pathway (i.e. the influence of the MOCES on ACMs) has been explored and widely described through electrophysiological recording of otoacoustic emissions (OAEs) in general and evoked OAEs (EOAEs) in particular (Bray, 1989; Collet et al., 1990; Kemp, 2002). EOAEs, produced in response to transient ipsilateral click stimulation, stem from linear reflections of mechanical irregularities in the cochlear sensory epithelium and are amplified by OHC electromotility (Shera and Guinan, 1999). They can be recorded as acoustic vibrations in the external auditory meatus (Bray, 1989; Kemp, 2002). Experimental results have shown that EOAE amplitude and auditory afferent activity decrease under contralateral auditory stimulation (Collet et al., 1990; Chabert et al., 2002), which is known to excite the MOCES (Collet et al., 1990; Giraud et al., 1995), as it does in animals under electrical stimulation of the crossed MOCB (Siegel and Kim, 1982; Cooper and Guinan, 2003). This strongly suggests that ACMs (i.e. OHC functioning) are modulated by MOCES activity in humans also. Based on these properties, non-invasive techniques, that can be applied clinically, have been developed to investigate both ACMs, using EOAE recording (Kemp, 2002), and the MOCES, using contralateral sound-induced suppression of EOAEs (Veuillet et al., 1999).
However, to date, the existence of a corticofugal system in humans, similar to that already described in animals (Huffman and Henson, 1990; Mulders and Robertson, 2000a; Doucet et al., 2003; Suga and Ma, 2003), remains speculative. There is only indirect evidence of any cortical modulation of cochlear functioning via the MOCES, provided by data on variability of MOCE activity, potentially linked to attention related cerebral activity (Giard et al., 1994), physiological hemispherical asymmetry (Khalfa et al., 1998), pathological cerebral abnormalities (Collet et al., 1993) or brain plasticity induced by musical training (Perrot et al., 1999). Recently, data on refractory temporal lobe epilepsy patients have shown post-surgical changes in MOCES activity (Khalfa et al., 2001), not only after superior temporal gyrus resection but also after anterior temporal lobectomy (including amygdalo-hippocampectomy), which are structures closely involved in auditory processing (Efron and Crandall, 1983). In addition, this corticofugal effect seemed to be stronger in the ear contralateral to the resection. Taken together, these results suggest a role of both the primary and the secondary auditory cortices in the modulation of peripheral auditory system activity and ACMs in humans.
As regards functional aspects, the perceptual correlates of MOCES activity in hearing remain a matter of debate. Experimental data in animals and humans suggest that this system could be involved in binaural phenomena (Liberman and Guinan, 1998; Pollak et al., 2003), in a reflex protecting activity of the inner ear from auditory fatigability and acoustic injury (Zheng et al., 1997; Rajan, 2000) and in auditory perception in noise (Kawase and Takasaka, 1995; Micheyl et al., 1997; May et al., 2004). Thus, corticofugal control of MOCES activity in humans may be of great importance, for both peripheral auditory system functioning and improved auditory signal processing, and especially for speech intelligibility under background noise (Giraud et al., 1997).
In this context, we sought to test the hypothesis of a direct influence of auditory cortex activity on cochlear functioning in humans by investigating ten epileptic patients suffering from medically refractory seizures, during the course of their presurgical chronic intra-cerebral electroencephalographic (EEG) assessment. This invasive approach to drug-refractory epilepsy (Spencer et al., 1993) is justified by the potential improvement in clinical course (Wiebe et al., 2001) and reduced mortality (Ryvlin, 2003) after ‘tailored cortical resection’, with a favorable benefit-to-risk ratio (Guénot et al., 2001). Direct intra-cerebral electrical stimulation (ICES) of the auditory cortex is included in the brain mapping of functional ‘eloquent’ cortex and epileptogenic areas (Rosenow and Lüders, 2001). Thus, our procedure did not add any invasive risk to the presurgical evaluation performed routinely in our department. Coupling this stimulation with EOAE recording in the opposite ear enabled the influence of the auditory cortex on ACMs to be assessed. Our hypothesis was that, if a descending auditory pathway exists, then contralateral auditory cortex ICES (‘contralateral’ referring to the opposite side to the ear where EOAEs were recorded) should, unlike stimulation of non-auditory contralateral areas, alter EOAE amplitude.
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Materials and Methods |
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Patients
Ten epileptic patients (five men, five women; mean age: 29 years) took part in this study (see Table 1). All but one were right-handed, according to the Edinburgh Handedness Inventory (Oldfield, 1971). All suffered from drug-resistant partial epilepsy and underwent a chronic intra-cranial electroencephalography during their presurgical assessment at the Neurological Hospital in Lyon, France. Mean age at onset of epilepsy was 12.1 years, with a mean duration of 16.6 years (range: 6.5–29.5 years). All but one had normal hearing and no previous history of otological disease; patient 4 (FR) had had chronic otitis media during childhood. At the time of the study, anti-epileptic drugs were tapered off in the majority of patients. According to French regulations for biomedical research in humans, our study was part of an invasive investigation with direct individual benefit. All the patients gave their fully informed consent to the presurgical assessment and for participating in the present investigation's protocol.
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Stereotactic Implantation of Depth Brain Electrodes
Brain structures to be explored were selected on the basis of clinical, electroencephalographic, morphological and functional neuroimaging data. The stereotactic implantation procedure used in this study was first described by Talairach and Bancaud (Talairach and Bancaud, 1973) and has been repeated since then (Liégeois-Chauvel et al., 1991; Ostrowsky et al., 2002). In broad outline, anatomical targets were located preoperatively on individual brain T1-weighted MRI and defined by stereotactic coordinates in a three-dimensional proportional grid system (Talairach and Tournoux, 1988). Depth brain electrodes were implanted perpendicular to the sagittal interhemispheric plane, after a cerebral angiography had been performed in order to prevent any vascular risk during implantation. Electrodes were 0.8 mm in diameter and each had 5, 10 or 15 active contacts of 2 mm in length, with an insulating gap of 1.5 mm between two adjacent contacts. The frontal and sagittal post-implantation teleradiography slices (acquired at the real size of the head) were superimposed on the corresponding individual morphological MRI slices (acquired at the real size of the brain), in order to enable the final location and stereotactic coordinates of the electrodes to be checked. Between 10 and 14 electrodes in each patient enabled stereoelectroencephalographic recording for up to 2 weeks, as well as cortical stimulation for functional brain mapping (Spencer et al., 1993).
Cortical Stimulation Paradigm
Detailed methodology has been described in a recent study (Ostrowsky et al., 2002). Intra-cerebral electrical stimuli were generated through a current-regulated neurostimulator designed for safe use in diagnostic stimulation of the human brain (Babb et al., 1980). Trains of electrical square pulses between two adjacent contacts were applied with the following parameters: high-frequency stimulation at 130 Hz, 0.3 ms pulse duration and 0.2 mA current intensity (charge density per square pulse < 10 µC/cm2), for 
64 s. In line with previous studies carried out in humans (Gordon et al., 1990; Velasco et al., 2000; Ostrowsky et al., 2002), these parameters of stimulation were chosen so as to ensure absolute safety regarding possible cerebral tissue injury. The use of a bipolar mode ensured more focused stimulation (Nathan et al., 1993). Functionally speaking, this high-frequency stimulation is thought to modulate cortical network activity by interfering with neural functioning (McIntyre et al., 2004).
Evoked Otoacoustic Emission Recording
Transient EOAEs were recorded according to the method developed by Bray and Kemp (Bray, 1989) and described elsewhere (Collet et al., 1990). Briefly, this consisted of measuring ear-canal sound pressure variations following transient acoustic stimulation, with a standardized recording ear-probe including both a transmitter and a miniaturized hypersensitive microphone. Sound stimuli were 80 µs non-filtered non-linear clicks, presented at a rate of 50 per s, with an intrameatal intensity of 77 ± 3 dB SPL peak-to-peak. Responses were acquired during the 20 ms interstimulus interval (including the first 2.6 ms related to stimulus resonance artifact) within a bandpass of 0.5–6 kHz. Each recording lasted 1 min, which corresponded to an averaging of 320 cochlear responses. After removing the first 2.6 ms of response to cancel the stimulus artifact, the EOAE amplitude was finally computed as the integral of the power of the waveform over the remaining 17.4 ms, expressed in dB SPL. The whole procedure was monitored by the Otodynamics ILO 88 system (v. 3.92 software).
Experimental Protocol
The procedure was carried out in the video-EEG unit as part of the functional brain mapping, at the end of the chronic intra-cerebral EEG monitoring. The patients, lying on their bed, were asked to relax and keep still. They were also asked not to move their eyes, either looking straight ahead or shutting their eyes, in order to avoid any visual bias related to an influence of gaze direction on central auditory system activity (Asbjornsen et al., 1990; Groh et al., 2001). As far as possible, the noise level in the vicinity of the patients' single rooms was kept to a minimum. EOAEs were recorded in the ear opposite to the ICES, i.e. in the right ear for left hemisphere stimulations and in the left ear for right hemisphere ones. The procedure comprised two sequences of two runs each: i.e. with and without ICES of, alternately, the auditory cortex or of a non-auditory area. In other words, the patients were tested without any cortical stimulation (‘WO’ condition), during electrical stimulation of either the primary or the secondary contralateral auditory cortex (‘AC’ condition) and during stimulation of a contralateral non-auditory area (‘NAA’ condition). For each patient, the identification of stimulated brain structures was performed through the same method as for the electrodes location. Primary and secondary auditory cortices, as well as non-auditory areas, were then anatomically defined on the basis of cytoarchitectonic (Galaburda and Sanides, 1980), electrophysiological (Liégeois-Chauvel et al., 1991), morphological and functional neuroimaging (Binder et al., 2000; Leonard et al., 1998) data in humans, with only the medial part of Heschl gyrus regarded as the primary auditory cortex. ICES began some s before the auditory click stimulation to allow time to check that there were no electrically-induced neurological symptoms and was applied throughout the EOAE recording, i.e. for 60 s. No specific synchronization was sought between the two stimuli, ICES and click. Recordings were obtained in random order. For eight of the patients, the whole procedure was repeated once. The procedure was carried out under video and stereoelectroencephalographic monitoring. During the protocol, the patients were unaware of the exact time of ICES.
Statistical Analysis
Distribution normality and equality of variance between groups were assessed by one-sample Kolmogorov–Smirnov test (with Lilliefors correction) and Levene's tests, respectively. Between-subject effects were tested using a Kruskal–Wallis test (analysis of variance on ranks) and within-subject effects using paired-sample t-tests. Differential effects of ICES on EOAE amplitude were assessed by comparing spontaneous variation (during the WO condition) and variation under electrical stimulation of either contralateral auditory cortex (the AC condition) or contralateral non-auditory area (the NAA condition). Spontaneous variation in EOAE amplitude was computed as the algebraic difference between the first and second without-ICES recordings. For all analyses, statistical significance was set at a probability level of P = 0.05.
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Results |
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Preliminary Analysis
Altogether, the ten epileptic patients were tested through recordings of 72 EOAE responses, either without any cortical stimulation or during ICES of 20 different cortical sites (see Fig. 1 and Table 2). Between-subject comparison of EOAE amplitude under the AC condition showed no statistically significant difference between primary and secondary auditory cortices stimulations on the one hand, and between right ear (under left auditory cortex ICES) and left ear (under right auditory cortex ICES) recordings on the other hand. Thus, all the AC condition data were pooled for analysis, irrespective of type of stimulated auditory cortex or side of tested ear. Similarly, for within-subject comparison, since there proved to be no significant difference in effect between the first and second sequences, the individual data for those patients who were tested twice were merged together for each condition, by means of a special program of the ILO software. This procedure enabled the signal-to-noise ratio to be enhanced for the EOAEs.
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Effect of Cortical Stimulation
In all patients, a reduction in EOAE amplitude was elicited by contralateral auditory cortex ICES (see Fig. 2), with a statistically significant difference between this electrically-induced amplitude variation under the AC condition and the spontaneous variation under the WO condition (paired t-test: t = –3.30, P = 0.009, two-tailed; see Table 3 and Fig. 3). Conversely, no significant change in EOAE amplitude was elicited under the NAA condition, by contralateral non-auditory area ICES (paired t-test: t = 0.67, P = 0.52, two-tailed; see Table 3 and Fig. 3). There was also a statistically significant difference in amplitude variation between the AC and NAA conditions (paired t-test: t = 4.95, P = 0.001, two-tailed; see Fig. 3). Moreover, the individual results for the eight patients tested twice showed adequate within-subject stability in the EOAE attenuation effect under auditory cortex ICES (see Fig. 4), and in EOAE amplitude without cortical stimulation.
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Control of Experimental Bias
To preclude the possibility that the reduction in EOAE amplitude was due to changes in EOAE recording conditions, such as changes in acoustic stimulation or middle-ear transfer function, both the click stimulus and the stimulus artifact were monitored. No statistically significant difference emerged across cortical stimulation conditions, either for acoustic stimulus intensity (paired t-test for non-auditory areas: t = 1.63, P = 0.14 and for auditory cortices: t = 0.67, P = 0.52, two-tailed; see Table 3) or for stimulus artifact amplitude (paired t-test for non-auditory areas: t = 0.22, P = 0.83 and for auditory cortex: t = –1.48, P = 0.17, two-tailed; see Table 3). Finally, it must be emphasized that, during our test procedure, none of the patients showed any clinical responses to ICES (such as auditory hallucinations or illusions) or electroencephalographic after-discharge (i.e. electrically induced seizure activity) (Lesser et al., 1984; Fish et al., 1993), even if such symptoms were sometimes elicited during other phases of the cortical mapping.
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Discussion |
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Corticofugal Modulation of Peripheral Auditory Activity
As the stability of the click stimulus intensity over the procedure rules out any technical bias linked to a modification in EOAE recording conditions, the EOAE amplitude change under auditory cortex ICES should be seen as a genuine effect. Physiologically, the reduction in EOAE amplitude stems from ACM inhibition by the MOCES (Siegel and Kim, 1982; Collet et al., 1990; Warr, 1992; Giraud et al., 1995). The present results thus confirm our main hypothesis and should be regarded as the first direct evidence of an auditory cortex influence on contralateral active cochlear micromechanisms, via MOCES-mediated modulation of OHC electromotility, in humans. This finding is in agreement with the corticofugal modulation of cochlear microphonic potential, principally reflecting OHC activity (Dallos et al., 1972), previously demonstrated in the mustached bat (Xiao and Suga, 2002a,b). Since we only tested the contralateral ear in this study, we cannot speak to the issue of asymmetry of this corticofugal effect, as suggested by experimental results in animals, showing stronger influences on the contralateral cochlea than on the ipsilateral one (Huffman and Henson, 1990; Warr, 1992; Torterolo et al., 1998; Xiao and Suga, 2002a).
Underlying Mechanism of Corticofugal Modulation
Though the corticofugal effect on contralateral cochlea must be mediated through a unique final pathway, represented by the medial olivocochlear efferent system (Warr, 1992; Mulders and Robertson, 2000a; Doucet et al., 2003), our results do not allow any further speculation on the precise anatomical structures relaying this descending auditory pathway. Besides, apart from the accepted MOCES suppression activity on peripheral auditory responses (Wiederhold and Kiang, 1970; Popelar et al., 2001), the corticofugal modulation depends not only on ICES effect on the auditory cortex, but also on basal cortico-olivary tonic activity (Xiao and Suga, 2002b). Valence of both ICES effect and cortico-olivary activity remains to be assessed. We can only assume that the successive stages of this experimental corticofugal effect are represented by a stimulation of cortical auditory neurons, causing spreading excitation or inhibition in adjacent cortical regions and modulation of the efferent activity of the subcortical auditory nuclei (Huffman and Henson, 1990; Doucet et al., 2003; McIntyre et al., 2004). Finally, the absence of auditory hallucinations during ICES of auditory cortex is not incompatible with a genuine effect of electrical stimulations on this area. Indeed, several experimental findings can explain this fact. On the one hand, the stimulation used in our study had a current intensity up to ten times lower and a pulse frequency twice as fast than those usually eliciting functional responses in epileptic patients (Lesser et al., 1984; Ostrowsky et al., 2002), especially for isocortical structures of the temporal lobe (Penfield and Perot, 1963; Fish et al., 1993). On the other hand, such high-frequency, low-intensity stimulations as those used in our study are likely to affect cortical functioning, e.g. by reducing epileptic activity in temporal lobe epilepsy patients, without inducing any clinical responses (Velasco et al., 2000). Thus, by analogy with transcranial magnetic stimulation of primary motor or visual cortex (Pascual-Leone et al., 1998; Kosslyn et al., 1999), and on the basis of the strength-duration relationship between threshold amplitude and stimulus duration (Kuncel and Grill, 2004), it is quite conceivable that ICES of auditory cortex (with a low pulse intensity but with a long duration of trains) should have locally altered cortical excitability without reaching perception threshold nor inducing auditory symptoms (McIntyre et al., 2004).
Alternative Interpretation of EOAE Attenuation Effect
As an alternative interpretation of our results, it could be argued that middle-ear muscles participated in the reduction in EOAE amplitude. Indeed, activation of the middle-ear reflex, mainly involving the stapedius muscle in humans (Borg et al., 1984), could lead to EOAE amplitude variations similar to those reported here. The underlying mechanism could be, on the one hand, a voluntary attentional or non-specific arousal effect on middle-ear reflex, and on the other, a corticofugal descending influence on the cochleo-stapedial loop (Liberman and Guinan, 1998; Mulders and Robertson, 2000b). The attentional or arousal hypothesis must be ruled out because the patients did not know when the cortical stimulation was applied. Since the results between the auditory cortices and non-auditory areas were different, even though the procedure was absolutely the same without and with ICES, and given that patients were unaware of the electrical stimulation, such an effect can hardly be assumed. The corticofugal descending influence hypothesis is supported by anatomical evidence in animals of connections between the medial superior olivary complex and the middle-ear reflex loop, which thus could be modulated by more central structures (Huffman and Henson, 1990). However, several experimental results seem to rule out this hypothesis. On the one hand, the fact that contralateral acoustic suppression of OAEs remains active in otoneurological patients in whom the middle-ear reflex has been abolished (Collet et al., 1990; Veuillet et al., 1991), whereas it is abolished or severely impaired in vestibular neurotomy patients with section of MOCB fibers (Williams et al., 1994; Giraud et al., 1995), is consistent with a genuine involvement of the MOCES. On the other hand, there was no significant variation in the amplitude of the acoustic stimulus artifact between EOAE recording with and without ICES. Briefly, the so-called EOAE waveform is made up of two acoustic responses: an initial fast decaying one (the ‘stimulus artifact’) and a delayed sustained one (the ‘EOAE’ proper) (Bray, 1989). Whereas EOAEs emanate from ACM (Shera and Guinan, 1999; Kemp, 2002), the stimulus artifact corresponds to a passive acoustic phenomenon arising from click resonance in the external auditory canal and the tympanic cavity, recorded during the first 2.6 ms of the acoustic response. A previous experimental study, carried out in normal hearing subjects, has shown that the stimulus artifact amplitude increased with positive as well as negative changes of ear-canal pressure, at the same time as spectral modifications of the EOAE waveform (Veuillet et al., 1992). By analogy with the principles of multifrequency tympanometry, these results strongly suggest an increase in the stiffness of the tympano-ossicular system in these pressure conditions (Colletti, 1977). We can thus rightly assume that the stimulus artifact indirectly reflects middle-ear transfer function and should vary with the contraction of the middle-ear muscles, if they are involved during our procedure (Veuillet et al., 1992). Thus, the stability of the stimulus artifact amplitude under ICES of the auditory cortex, coupled with the decrease in EOAE amplitude, runs counter to any involvement of the middle-ear in this effect. Taken together, these data argue against the involvement of the middle-ear reflex in the EOAE attenuation effect observed under electrical stimulation of the auditory cortex.
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Conclusion |
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To conclude, our findings highlight a direct functional interaction between contralateral cortical auditory areas and the peripheral auditory organ in humans. Each level of the auditory system, from the periphery to subcortical nuclei, may then be under a top-down control of corticofugal descending auditory pathways, likely to improve auditory signal processing even in the early stages of the peripheral auditory system.
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Acknowledgments |
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The authors are grateful to A. Moulin and E. Veuillet for technical assistance, and to the staff members of the video-EEG and SEEG unit for their kind help.
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References |
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