May - August 2005: Suppression of Otoacoustic Emissionsand the Efferent Auditory System. General thoughts and clinical Applications.
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- Written by Panagiota Lalaki , MD, PhD
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Introduction
In 1946, Grant Rasmussen reported his discovery of the olivocochlear (OC) system. Warr and Guinan (1979) anatomically outlined the two separate segments of the OC system, the lateral and the medial. An efferent auditory pathway can be found in all cases of vertebrates. In human, the efferent auditory pathway is completely mature by 40 weeks after gestation (Ryan και Piron,1994). Morlet et al., (1993) have reported abnormal function of the OC bundle in a study of 42 premature infants (33-39 weeks). Its functional role remains largely unknown.
The two efferent divisions differ with respect to a number of morphological features, including (Sahley et al., 1997a):
1. pattern of development,
2. the size of cell bodies,
3. brainstem locus of origin,
4. preferred side of projection to the periphery,
5. postsynaptic targets within the auditory periphery
The descending (efferent) OC system is known to have cell bodies and axons originating from nuclei within the superior olivary region in the upper pons (superior olivary complex-SOC). The descending fiber bundles provide direct, bilateral input to the cochlea via anatomically segregated medial and lateral efferent divisions (Warr 1992). All available evidence indicates that the dynamic properties of the Outer Hair Cells (OHCs) fall under the modulatory control of the medial efferent auditory system (Kujawa et al., 1993,1994; Collet et al. 1992; Gifford & Guinan 1987).
Clinical interest in the medial efferent system has been awakened by the advances made in the field of Otoacoustic Emissions (OAEs). Since the micromechanical properties of the OHCs are directly under the control of the medial efferent bundle, it sounds logical that stimulating this neural pathway, OHCs motility and, hence, OAEs should be affected. It is well established that the amplitude of both types of Evoked Otoacoustic Emissions (TEOAEs as well as the Distortion Product Otoacoustic Emissions-DPOAEs) can be suppressed when simultaneous contralateral sound stimulation is applied (Williams et al., 1994; Moulin et al., 1993; Ryan et al., 1991). This phenomenon is considered to be mediated through the medial efferent system (Williams et al., 1994).
Overview of the efferent auditory system neuroanatomy
The efferent auditory system is a descending bundle, which originates from the auditory cortex and terminates at the sensory cells of the organ of Corti. Throughout its descending course the efferent auditory pathway interacts with the afferent auditory pathway through feedback loops.
The olivocochlear bundle
In 1946, G. Rasmussen reported his discovery of the OC bundle. Warr (1992) and Warr & Guinan (1979) outlined two separate anatomic segments of the efferent auditory system, the lateral and medial.
The lateral OC bundle arises from neurons within the Lateral Superior Olivary (LSO) nucleus complex in the upper pons and its unmyelinated axons terminate to the inner hair cells (ICHs) mainly (89%-91%) of the ipsilateral cochlea. They do not synapse directly at the basal surface of the IHCs but at specialized postsynaptic regions on afferent type I dendrites (Pujol & Lenoir 1986).
The medial OC bundle arises from the neurons of the Medial Superior Olivary (MSO) nucleus complex and the Medial Nucleus of the Trapezoid Body (MNTB) and comprises of thick myelinated nerve fibers. About 75% of the fibers cross at the floor of the 4th ventricle and terminate at the OHCs of the contralateral cochlea, while the rest of them remain uncrossed and terminate to the OHCs of the ipsilateral cochlea. The fibers of the medial OC bundle synapse directly at the basal surface of the OHCs. Figure 1 schematically illustrates the olivocochlear bundle and its connections with the cochlear nucleus and hair cells within the cochlea.
Figure 1: Schematic presentation of the efferent auditory system and its connections to the afferent auditory system and the hair cells of the organ of Corti.
Both the lateral and medial fibers of the OC bundle pass dorsally from their cell bodies through the reticular formation to the floor of the 4th ventricle (Warr 1992). Together with the crossed vestibular efferents, descending auditory efferent axons form a compact bundle within the vestibular nerve root, the fibers pass the cochlear nuclei and send collateral projections into this structure before exiting the brainstem as a ventral component of the inferior division of the vestibular nerve (Warr 1992). Efferent fibers travel within the vestibular nerve, then enter the cochlea between the basal and second turn and enter the spiral ganglion, via the vestibulocochlear anastomosis of Oort in the fundus of the internal auditory meatus (Warr 1992; Iurato 1974).
Descending pathways to the superior olivary complex
Descending auditory pathways arise from within the auditory cortex -the primary (AI) and secondary (AII) auditory field as well as the anterior auditory field (AAF)- through which the cortex may exert control over the superior olivary neurons of the efferent OC bundle. This descending control is indirect, via connections mostly with the ipsilateral inferior colliculi (IC). Limited amount of existing evidence suggests that descending fibers from the IC terminate on the cells of the SOC and MNTB. Furthermore, the descending collicular input to the SOC and MNTB is found to be tonotopic, which supports electrophysiological evidence (Rajan 1990) that descending collicular input is very capable of modulating levels of excitability within medial efferent OC neurons (Kimiskidis et al., 2004; Sahley et al., 1997b).
SOC interactions with the cochlear nucleus
Descending fiber projections arise from the SOC bilaterally, travel within the intermediate and dorsal acoustic stria and terminate within the cochlear nuclei. Fibers from LSO complex mainly terminate to the ipsilateral ventral cochlear nucleus (VCN) and, vice versa, afferent fibers from the VCN project to the ipsilateral LSO complex. A dense plexus from the MSO complex send fibers that terminate to the ipsilateral and mainly to the contralateral dorsal and ventral cochlear nuclei. Furthermore, afferent auditory fibers from the cochlear nuclei project mainly to the contralateral MSO nuclei (Sahley et al., 1997b). Thus, most medial OC nuclei are activated by the contralateral cochlea they innervate, and most lateral OC nuclei are excited by ipsilateral cochlear output. There exists, therefore, a neural pathway from one cochlea via the afferent auditory system to the MSO nuclei, and from there to the other cochlea via the medial efferent auditory system (fig. 2).
Figure 2:Schematic presentation of contralateral suppression emission test and the neural pathways (afferent and efferent auditory system) being activated. Overall TEOAE amplitude without contralateral noise is at 16.3 dB SPL; when white noise is presented to the contralateral ear the overall amplitude is suppressed to 8.3 dB SPL. (MSO: medial superior olivary, CN: cochlear nucleus, SL: sensation level).
The role and clinical relevance of the efferent auditory system
The role of the efferent auditory system remains largely unknown. In view of the preferential innervation of the OHCs by MSO fibers, it has been hypothesized that the stimulation of the medial efferents alters IHCs sensitivity indirectly by altering the micromechanical properties of the OHCs. It is well established that the length, tension and the stiffness of the OHCs along their longitudinal axis are under the control of the MOC bundle, thus enhancing the auditory sensitivity, especially for low level stimuli at 30-40 dB SL (Brownell 1990; Guinan 1986; Kim 1986; Siegel & Kim, 1982).
There is some evidence suggesting that the medial efferent system enhances the frequency resolving capacity (Micheyl & Collet, 1996; Igarashi et al., 1979) and the vowel discrimination, especially in a background of noisy environment (Muchnik et al., 2004; Sahley et al., 1997c). Furthermore, Tolbert et al. (1982) support the idea that the OC bundle optimizes the detection of interaural intensity differences for higher frequency signals by increasing, within the cochlea, the interaural disparity reaching the LSO. Therefore, better understanding of the significance of the medial efferent system and its pharmacological manipulation may prove beneficial for children and adults who have difficulties in speech discrimination in noisy environment (classroom etc), despite normal pure tone audiometric thresholds, as well as for subjects exposed to intense occupational noise.
Several studies have provided evidence suggesting that activation of the medial efferents serves a protective function in the mammalian auditory periphery against high-level auditory stimuli (Canlon 1996; Subramanian et al., 1993; Liberman 1991).
Since the medial olivocochlear bundle is mainly inhibitory, there has been already suggestions that dysfunction of the efferent auditory system, at any level from auditory cortex to cochlea, may be a basis for tinnitus generation, especially in noise-induced tinnitus cases (Prasher et al., 2001; Attias et al., 1996) and in tinnitus after head injury (Ceranic et al, 1998).
It has been also suggested that hyperacusis might be associated with dysfunction of the efferent system, as estimated by the abnormal OAEs suppression and the extreme high prevalence of recordable multiple SOAEs (Ceranic et al., 1998).
Suppression of OAEs
Because descending medial efferent fibers preferentially terminate on OHCs, the prevailing view is that the micromechanical properties of the OHCs are in direct control of the efferent innervation. Since OAEs is thought to reflect these dynamic properties, it has been hypothesized that activating the medial efferents would produce alterations to cochlear micromechanics and, hence, to OAEs. Indeed, there is now great body of evidence that auditory sound stimulation, presented ipsilaterally (Tavartkilage et al., 1997) or contralaterally, results in reduction of the amplitude of both types of Evoked OAEs (TEOAEs and DPOAEs) (Moulin et al., 1993; Ryan et al., 1991; Collet et al., 1990). This phenomenon is called suppression of OAEs and it is proved that is mediated through the medial efferent system (Williams et al., 1994; Kujawa et al., 1993; Veuillet et al., 1991; Warren & Liberman 1989).
Thus, it has been suggested that the contralateral suppression of OAEs could serve as an objective, non-invasive clinical test for the exploration of the non-linear micromechanics of OHCs and the clinical neurologic evaluation of the auditory brainstem in general and descending efferent bundle, specifically.
How to perform the suppression test?
As mentioned before, both types of evoked OAEs (TEOAEs and DPOAEs), can be suppressed when auditory stimulus is applied either to the ipsilateral or the contralateral ear. Contralateral suppression is more commonly used in both clinical and experimental projects. Ipsilateral suppression of TEOAEs has been studied by G. Tavartkiladge et al., (1997), but special equipment (probe) is needed and, as stated by the authors, suppression of TEOAEs could not be attributed only to the medial OC bundle but to intracochlear processes, as well.
The optimum parameters for performing the contralateral TEOAEs suppression test were found to be as follows (fig. 2):
1. stimulus for TEOAEs generation: linear-clicks at approximately 60 dB SPL (±3 dB peak SPL), duration 80 μs and repetition rate of 50s-1.
2. contralateral sound stimulation: white noise at low intensity (30-50 dB SL) (Berlin et al, 1994; Ryan et al, 1991), so that any crossover phenomenon and contraction of the contralateral stapedius muscle is avoided. Some authors suggest that the contralateral sound stimulus should be presented at intensities of 10-15 dB lower than the threshold of contralateral acoustic reflex, elicited by white noise (Williams et al, 1994).
3. collection and analysis of data: Ten runs of 60 sweeps each are averaged alternately with and without contralateral white noise stimulus. Thus, 5 alternate buffers were combined to give an average of 300 sweeps each. The difference between the amplitude in dB SPL of the total response without contralateral noise and that with contralateral noise is measured as the degree of suppression of TEOAEs (Prasher et al, 1994).
The suppression of TEOAEs in normal hearing adults shows a great intra-individual variability, but, according to several studies, 1 dB SPL is considered to be the “cut-off” point for normal medial OC bundle function (Prasher et al., 1994; Collet, 1993). Considering 1 dB SPL as the lowest “normal” level, the method shows a false positive rate of 6% (Prasher et al, 1994) in normal hearing subjects, and a false negative rate of 17% and 0% in cerebellopontine angle tumors and intrinsic pontine lesions, respectively.
The suppression of DPOAEs has been studied mainly in experimental animal projects. Moulin et al (1993) propose the following parameters as optimal for this test:
1. stimulus for DPOAEs generation: primary tones at low level (L1=L2=50-60 dB SPL).
2. contralateral sound stimulation: white noise at a minimum intensity of 30 db SL.
DPOAEs are suppressed throughout their frequency range, the maximum suppression being at frequencies from 0.5 to 2 kHz (Moulin et al., 1993). DPOAEs suppression shows frequency specificity if narrow-band noise is used as a contralateral stimulus (Chery-Croze et al., 1993).
In conclusion, simultaneous contralateral sound stimulation results in the following changes in OAEs (SOAEs, TEOAEs and DPOAEs) (Collet 1993):
1. Reduction of the overall amplitude of at least 1 dB SPL.
2. Phase shift.
3. The suppression effect becomes greater when the intensity of contralateral noise increases (greater suppression is reported at an intensity of 50 dB SPL).
4. The degree of TEOAE and DPOAE suppression becomes greater as the level of the ipsilateral stimulation decreases (greater TEOAEs suppression is reported with clicks at an intensity of 60 ± 3 dB SPL and greater DPOAEs suppression with low-level primary tones).
Influence of maturation and ageing
In preterm babies (up to 40 weeks of gestation) no suppressive effect has been evidenced (Morlet et al., 1993), due to immaturity of the efferent auditory pathway. In fullterm babies a slight effect has been shown (Ryan et al., 1994). In the elderly, the suppressive effect is present but smaller than in young adults (Castor et al., 1994).
Influence of sleep
OAEs suppression occur during sleep whatever the stages, but in almost half of the subjects no effect is seen at the onset of sleep during 15 minutes (Froehlich et al., 1993).
OAEs suppression in clinical applications
OAEs is the only objective and non-invasive method for the evaluation of the functional integrity of the medial efferent system, and, therefore, for the evaluation of the structures lying along its course, at least up to the level of inferior colliculi (VIII nerve, cerebellopontine angle and pons).
Diagnosis of extrinsic and intrinsic pontine lesions
Although, literature data are rather poor, there is evidence that the efferent test could be useful in the diagnosis of pontine lesions either extrinsic (acoustic neuromas, meninigiomas, congenital cholesteatomas) or intrinsic (multiple sclerosis, ischemic infarcts, tumors). Prasher et al. (1994) conducted a study in 18 patients suffering cerebellopontine angle (CPA) tumors and 11 patients with intrinsic pontine lesions. According to their results, 15 out of 18 patients with CPA tumors demonstrated abnormal TEOAE suppression ipsilateral to the lesion. The suppression was abnormal in all patients suffering intrinsic pontine lesions.
The author performed the TEOAE suppression test in a group of 11 patients with CPA tumors (6 with acoustic neuroma, 1 congenital cholesteatoma, 3 meningioma, 1 lipoma) and a second group comprised of 21 patients suffering intrinsic pontine lesions (10 with multiple sclerosis, 7 ischemic infarct, 1 pontine hemorrhage and 3 tumors). A third group of 20 young healthy, normal hearing volunteers served as the control group for the TEOAE suppression test. Normal suppression (³1 dB SPL) demonstrated 18 out of the 20 controls (false positive rate 6.7%). All patients with CPA tumors showed abnormal suppression (<1 dB SPL), either ipsilaterally to the lesion or bilaterally (sensitivity 100%). Bilateral abnormal suppression was found whenever pressure was exerted on the pons due to the size of the tumor. Abnormal suppression was recorded in 17 out of 21 patients of the intrinsic pontine lesions (sensitivity 81%).
Figures 3 and 4 illustrate characteristic cases of abnormal TEOAE suppression in pontine demyelinating disease and CPA tumor, respectively.
Figure 3 TEOAE suppression test in a case of a 30 year-old man complaining of different sound pitch perception from his left ear. Pure tone audiometry was within normal limits, TEOAEs were recorded with normal amplitude and repro- bilaterally but he lacked suppression of the emissions from both ears. MRI revealed a demyelinating lesion in the course of the VIII into the pons.
Figure 4: TEOAEs suppression test in a case of a 51 year-old woman suffering a CPA meningioma on the right (MRI). She had a mild to moderate sensorineural hearing loss, normal OAEs and abnormal suppression bilaterally, presumably due to the pressure exerted on the brainstem by the tumor.
Auditory neuropathy
Auditory neuropathy is a clinical entity that has drawn the interest of audiologists the last few years. It is characterized by sensorineural hearing loss in pure tone audiometry, speech discrimination difficulty, absence of acoustic reflexes, normal OAEs and absent or severely abnormal auditory brainstem responses (ABR) without any radiologically evident retrocochlear lesion. The age of patients range from infancy to adulthood and it could present as a neuropathy of the VIII nerve alone or, most frequently, as a part of hereditary motor sensory neuropathies (i.e. Charcot-Marie-Tooth syndrome, Freidreich’s ataxia syndrome) (Doyle et al., 1998; Starr et al., 1996) Auditory neuropathy patients lack suppression of OAEs (Hood et al., 2003; Lalaki 2003; Abdala et al,. 2000).
In conclusion, there exists evidence that the assessment of the medial olivocochlear system by recording OAEs under contralateral acoustic stimulation in a suspected lesion of the CNS could contribute to neuro-otological topographic diagnostics. It could be performed complementary to Auditory Evoked Brainstem Responses (ABR) or in cases with mean hearing threshold worse than 60 dB HL where the ABR test is of limited sensitivity (provided that TEOAEs could be recorded due to the retrocochlear nature of the hearing loss).
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About the Author
Panagiota lalaki MD, PhD is an expert of OAE suppression and clinical applications . She is an active member of the Portal's web Editorial Board.