| [Download PDF]
|Year : 2001 | Volume
| Issue : 12 | Page : 61--73
Objective evidence for tinnitus from spontaneous emission variability
D Prasher1, B Ceranic2, W Sulkowski3, W Guzek3,
1 Institute of Laryngology and Otology, University College, London, United Kingdom
2 National Hospital for Neurology and Neurosurgery, London, United Kingdom
3 ENT & Audiology Division, The Nofer Institute of Occupational Medicine, Lodz, Poland
Institute of Laryngology and Otology, University College London,330 Gray’s Inn Road, London WC1X 8EE
Noise exposure is the most common cause for the generation of tinnitus. This study evaluated the variability of spontaneous emissions in industrial workers exposed to noise and reporting the presence of tinnitus in comparison with those exposed to noise but without tinnitus. The assumption being that exposure to noise leads to some instability within the cochlea, which alters the spontaneous emission activity. Thus those experiencing tinnitus may show greater variability than those without tinnitus.
198 mill workers in Poland exposed to noise levels between 85-95dBA for a mean of 12+6.6 years, 104 of whom had reported the presence tinnitus and 94 without tinnitus were evaluated for otoscopy, audiometry and otoacoustic emissions. The tests were repeated between 5-10 days in most subjects to check for variability.
There were significant differences in the mean age, pure tone average, transient emissions amplitude and variability between groups with and without tinnitus. There were no significant differences between sessions for these measures in either group.
Those with tinnitus had poorer thresholds by an average of around 15dB, and reduced TOAE of around 2.6dB compared with those without tinnitus. There are a number of factors such as age, pure tone thresholds and tinntius, which may be responsible for the reduction in emissions.
For the purposes of examining SOAE stability, all SOAE peaks were classed as stable if SOAE frequency in the two sessions remained unchanged and variable if SOAE peaks were present in both sessions but shifted in frequency or present in one sessions and absent in the other. SOAE were present in 73.1% of tinnitus group and in 50% of non- tinnitus group. Of these 92% of the tinnitus group had present and variable SOAE whereas 48.9% of the non-tinnitus group did. Thus the positive predictive value was calculated at 65% for those with variable SOAE having tinnitus and significantly higher at 86% negative predictive value for those with stable SOAE having no tinntus.
The likelihood ratio of tinnitus being present given that SOAE are present and variable is 1.87 and is significantly reduced for no tinnitus given that SOAE are present and stable at 0.156. This study has clearly demonstrated that the incidence of spontaneous emissions is higher in noise-exposed workers than previously observed and the stability from week to week is significantly lower in those with subjective tinnitus.
|How to cite this article:|
Prasher D, Ceranic B, Sulkowski W, Guzek W. Objective evidence for tinnitus from spontaneous emission variability.Noise Health 2001;3:61-73
|How to cite this URL:|
Prasher D, Ceranic B, Sulkowski W, Guzek W. Objective evidence for tinnitus from spontaneous emission variability. Noise Health [serial online] 2001 [cited 2022 Oct 3 ];3:61-73
Available from: https://www.noiseandhealth.org/text.asp?2001/3/12/61/31796
Tinnitus is the perception of a sound in the absence of any external stimulation. It is a symptom of different pathophysiological states of the ear and the central nervous system. The large variation in tinnitus masking patterns and differences in the efficacy of treatments implies that tinnitus may be generated at different levels of the auditory system and may result from different underlying mechanisms.
The epidemiological evidence (Coles, 1984) indicates that 15% of the UK population may have tinnitus without any temporary cause such as noise or drugs, in 8% or so it may interfere with sleep and in 0.5% it may severely affect normal life. Similar values have been reported by others in Europe (Axelsson and Ringdahl, 1987; Quaranta, 1996) and in the USA (Cooper, 1994). It is present in women more than in men, in the left ear more than in the right ear and in greater numbers with increasing age.
Mechanisms of generation
The underlying mechanism for the phenomenon of tinnitus is poorly understood. Tinnitus is often associated with hearing loss or ear disease but it is possible for an abnormality, which may result in the presence of tinnitus to occur at any level in the auditory pathway. The nature of the processes involved may vary according to the level at which the abnormality occurs but having the same effect in terms of the tinnitus experienced by the subject.
Several neuro-physiological mechanisms have been proposed including 'cross-talk' of neighbouring fibres (Moller, 1984; Moller and co-workers, 1992), gate control hypothesis (Tonndorf, 1987), heterogeneous activation of the efferent pathway (Hazell, 1995). Increased neuronal activity resulting from pathological signals in the auditory pathway has been suggested as a possible cause of the generation of tinnitus (Jastreboff, 1994).
The role of cochlear mechanics in the generation of tinnitus was anticipated by Gold (1948). He speculated that "ringing" in the ear originates in spontaneous mechanical oscillation of the physiologically active feedback mechanisms situated within the cochlea. This hypothesis has been supported by the introduction of otoacoustic emission techniques (Kemp, 1978), which have allowed the examination of cochlear mechanics. Since then, there have been a number of single case reports linking tinnitus with spontaneous otoacoustic emissions. Changes in spontaneous emissions have been associated with the subjective alterations in the perceived sensation of tinnitus.
Tinnitus may be evoked by external sounds such as noise exposure, which acts as a source of energy to set the cochlea into a state of mechanical instability and sustained oscillations. Kemp (1982) demonstrated a biphasic effect of noise exposure, initially showing a reduction in cochlear emissions followed by an enhancement of micro-mechanical cochlear activity coinciding with post-noise exposure tinnitus.
It has also been proposed (Pujol et al., 1993; Brix et al., 1996) that tinnitus could be generated in cochlear synapses between the inner haircells and afferent neurons as a result of glutamergic neuro-toxicity. The subsequent disturbed synchronisation of the peripheral stimulusrelated evoked activity could be a basis for tinnitus.
The feedback interaction between the cochlea and central auditory structures is another possible mechanism for the generation of tinnitus. The high density of the efferent olivocochlear innervation of outer haircells (OHCs) is an expression of the potential influence of the efferent system on cochlear mechanics. This effect is far from fully understood, but it is considered to be predominantly suppressive. The higher structures in the auditory system can modulate the excitability of olivocochlear neurons or cortical and subcortical pathways and subsequently may also alter cochlear mechanics. This function raises the possibility of efferent activity having an important role in tinnitus generation.It has been postulated that a partial cochlear lesion , for example, due to noise exposure may trigger heterogeneous activation of the efferent system. Of particular importance is thought to be partial OHC lesion in the presence of intact inner hair cells (IHCs), so called discordant damage or functional dissociation of OHCs and IHCs (Jastreboff, 1990). A partial OHC lesion leads to reduced afferent input, which in turn leads to "overactivity" of the intact OHC near the lesion, as a result of the feedback response of the efferent system to increased afferent input from the damaged region. This in turn brings about an "overspill" effect in to the intact neighbouring OHCs. This hypothesis finds support in the common observation that tinnitus pitch corresponds to the slope of hearing loss (Penner, 1980)
Different morphological and neurophysiological changes in the central auditory system following a cochlear lesion, for example, due to noise exposure, have been observed (Salvi et al., 1992). These changes, which may be of relevance in the generation of tinnitus, do not simply mirror peripheral damage. Cochlear lesions alter the activity in the auditory nerve and increase excitability of the cochlea nucleus, inferior colliculus, and medial geniculate body. Since the IC is the obligatory relay for the ascending auditory pathway, this may cause an imbalance between the excitatory and inhibitory mechanisms, mediated by the neurotransmitters of the auditory pathways, such as glutamate, glycine, acetylcholine, or gamma-amino-butyric acid (GABA).
Studies of the auditory cortical neurons have indicated changes in their frequency selectivity. Reduced afferent input due to a cochlear lesion, initiates a sequence of changes in the relative levels of excitatory and inhibitory inputs to the primary auditory cortical neurons. This leads to expansion of the receptive field (located in the cochlea, adjacent to the damaged region) of the cortical neurons (Rajan et al., 1992), which in turn raises the threshold sensitivity and broadens frequency selectivity. Restricted damage to the cochlea also produces a tonotopic reorganisation of the receptor surface in the primary auditory cortex. The area in the auditory cortex deprived of its characteristic frequency peripheral input acquires a new characteristic frequency, of that at the edge of the region of the cochlear damage (Schwaber et al., 1993). In other words, the damage to the cochlea leads to an expansion of the cortical representation of a restricted frequency band adjacent to the region of the cochlear loss. Such plasticity of frequency selectivity and auditory maps may alter perceptual function, and therefore may contribute to the generation of tinnitus.
The neurophysiological concept of tinnitus generation assumes active involvement of the central auditory and other central nervous systems mechanisms. A mechanism proposed by Jastreboff and Hazell (1993) implicates a pathological signal in the auditory system triggering a sequence of events, resulting in increased neuronal activity at different levels of the auditory pathway, which may be perceived as tinnitus. However, other systems , particularly, the limbic and autonomic nervous systems are thought to be essential for the emergence of and preservation of the "phantom" sound, tinnitus.
Moller and co-workers (1992) suggest that tinnitus results from pathological synchronized (phase-locked) neural activity in the auditory nerve, for example due to abnormal communication, cross talk or ephatic transmission between neighbouring auditory nerve fibres following the damage to the myelin sheath.
Another possible is the interaction between the auditory and other sensory/motor system, for example visual, such as occurring in gaze evoked tinnitus, due to synaptogenesis and cortical organisation, following unilateral deafferentation of the auditory periphery. In some forms of tinnitus, an interaction between auditory and extralemniscal multi-sensory pathways may occur, such as in tinnitus induced by electrical stimulation of somatosensory system.
Previous work on Otoacoustic Emissions and Tinnitus
Currently the role of otoacoustic emissions (OAEs) in the evaluation of tinnitus, as a part of the neuro-otological assessment, is primarily to establish cochlear integrity and to detect early outer haircell damage, using transient evoked otoacoustic emissions(TEOAEs). This method is gaining an increasing importance in clinical practice. Less frequently applied is the method of assessment of olivo-cochlear suppression by recording of TOAEs under contralateral acoustic stimulation (Veuillet et al., 1992; Chery-Croze et al., 1994) to identify efferently mediated mechanisms underlying tinnitus. This method is not yet accepted as a routine test as its significance is not fully understood and it lacks sufficient normative data. There have been a few attempts to employ OAEs in the authentication of the presence of tinnitus, which have resulted in the observation of the difference between tinnitus and non-tinnitus patients. These are probably consequences of the differences in the degree of outer haircell lesions(Mitchell et al., 1996; Janssen et al., 1996).
The relationship between spontaneous otoacoustic emissions (SOAEs) and tinnitus has been studied extensively. Two reviews (Norton et al., 1990; Penner, 1992) provide details of individual work. [Table 1] summarises the data currently available and highlights patients in whom tinnitus was considered to be related to SOAEs. A number of different experiemental criteria have been applied to link tinnitus with SOAEs, the most common being the correspondence of tinnitus pitch and the frequency components of SOAEs. Other critera include the simple co-existence of tinnitus and SOAE; recording of emissions and on subsequent playback, identification of SOAE frequency as the pitch of tinnitus; the effect of interaction of SOAE and mechanical/acoustic stimuli on the audibility of tinnitus. A set of criteria for establishing a relationship between tinnitus and SOAE have been proposed by Penner and Burns 1987. These are (i) correlation of tinnitus pitch with SOAE frequency , (ii) suppression of SOAE making tinnitus inaudible, (iii) masking of tinnitus abolishing SOAE, (iv) frequency specific isomasking contours of tinnitus. Although, in general, the attempts to attribute tinnitus to SOAEs have been disappointing, there are some patients with convincing evidence of a close correspondence between tinnitus and SOAEs (Penner, 1988,1989,1990, Coles, 1996). The true prevalence of SOAE-related tinnitus remains unknown, Moreover, the subjects examined in the reviewed studies , most of them case studies, constitue a heterogeneous group with respect to age, aetiology, and audiometric patterns and therefore the existence of the SOAE-related tinnitus and its prevalence in any single aetiological group of patients with tinnitus remains undetermined.
It appears that tinnitus and SOAEs may be related but no definite conclusion can be drawn in the absence of any large study with universally agreed diagnostic criteria and clearly defined groups of subjects.
Our Studies on Emissions and Tinnitus
Our previous work (Prasher, et al., 1994; Prasher et al., 1995) has shown that efferent suppression of transient otoacoustic emissions is significantly reduced in patients with brainstem lesions affecting the auditory pathway. In addition, we have shown that spontaneous emissions have an increased variability over time in subjects with tinnitus (Ceranic et al., 1998a).
Study 1: Spontaneous Emissions and Tinnitus in four aetiological groups
In the initial study, 20 control subjects with SOAEs were selected from 38 volunteers and 53 subjects with tinnitus from 100 consecutive patients seen. The patients were from five aetiological groups namely, those with normal hearing (20), abnormal hearing (10), head injury (10), Meniere's disease (10), and noise exposure (3). The SOAE stability was categorised as "stable" if unchanged on repeat testing, "shifted" if SOAE peaks were present in the two sessions but shifted in frequency and "on-off" if present in one session but absent in the other. In comparison with the control group, the tinnitus group showed statistically significant lower reproducibility of SOAE peaks in the tinnitus group: the number of "stable" SOAE peaks in the tinnitus group was 23.8% compared to the control of 58.2% while the number of "on-off"peaks was significantly higher statistically in the tinnitus group, 47.3% compared to 5.5% for controls. The number of "shifted" SOAE peaks was not significantly different between the two groups but the magnitude of frequency shifting, expressed as relative frequency shift was significantly higher in the tinnitus group (0.59% compared to 0.25% in controls), which was particularly so in the head injury subgroup (0.84%).
The prevalence of SOAE in the control and tinnitus group was very similar. These findings suggest that the variability of SOAEs is, in a significant number of subjects, associated with the complaint of tinnitus. SOAEs are, in general, thought to arise as a response to random perturbations in cochlear mechanics due to inherent irregularities in OHC arrangement. In normal subjects, in whom cochlear structural arrangement and functional capacity remain unchanged, and control mechanisms are well balanced, there is no reason for changes in SOAEs, and this confirmed by the finding of stable SOAEs. These weak narrow-band signals, due to their continuous presence, are subject to perceptual adaptation and are, therefore inaudible. Unstable SOAEs may correspond to the unstable cochlear mechanics due to some local causes, resulting from mutual interaction of multiple peaks, changes in middle ear transfer properties, and various external (acoustic, mechanical) and internal factors. However, variable SOAEs, may also reflect instability of the higher central nervous structures. The effect of the central auditory system on cochlear mechanics may be exerted through efferenty induced mechanisms of electro-mechanical transduction, which may alter the gain in the feedback loop of a cochlear amplifier and further, the SOAE frequency spectrum. This may find support in the observation of significantly higher inter-session variability of the medial olivo-cochlear suppression in patients with tinnitus compared with normal subjects.It is possible for disinhibition of the efferent suppression due to central auditory system dysfunction to lead to an increase in cochlear output and consequently to the occurrence of unstable SOAE. This is supported by the findings observed in the head injury group in particular with the highest prevalence of unstable SOAEs due to undamped cochlear activity subsequent to central efferent disinhibition following head injury. The differences in the prevalence of SOAE between the subgroups emphasises the importance of studying tinnitus in aetiologically homogeneous groups, to identify group-characteristics as a consequence of particular underlying mechanisms.
Study 2: Emissions and Tinnitus after Head Injury
In a further study (Ceranic et al., 1998b), subjects with head injury but with and without tinnitus were tested, showing significantly increased TOAE amplitude in those with head injury and tinnitus (12.8dBSPL) in comparison with controls (8.0dBSPL) and those with head injury but no tinnitus (6.2dBSPL). The SOAE prevalence in subjects with head injury and tinnitus was significantly different at 100% (with a mean of 4.4 peaks per ear) compared to 17% with head injury but no tinnitus (0.25 peaks) and 50% in normal subjects (1.7 peaks). In addition, 43% of subjects with head injury and tinnitus had absent suppression of TOAE ( Study 3: Emissions and Tinnitus after Noise Exposure
In this study it is assumed that exposure to loud noise results in some instability within the cochlea, which leads to the sensation of tinnitus and the presence of spontaneous emissions. The objectives of research were to (i) evaluate the relationship between spontaneous emissions and noise induced tinnitus, (ii) determine the variability of spontaneous emissions as a possible indicator of the presence of tinnitus by examining groups of noise exposed workers with and without subjective tinnitus.
Subjects were recruited from two factories in Lodz, Poland. The noise levels ranged from 8595dBA. The occupational physician at each factory asked the subjects to participate in the study. There were 104 subjects (39 females, 65 males) who had reported the presence of tinnitus and 94 (41 females and 53 males) who had experienced no tinnitus. The mean age of subjects with tinnitus was 47+9 years whereas that for the subjects without tinnitus was 39+9 years. Each subject was asked a series of questions regarding their tinnitus and work and medical history.
The following tests were conducted.
Otoscopy: Subject's ear canal and drum were examined and if free from wax and any other abnormality, were referred for further testing.
Tympanometry: Middle ear was examined for tympanic membrane mobility in relation to change in pressure.
Audiometry: Standard pure tone audiometry was carried out in a sound proof booth to determine auditory threshold at octave frequencies from 125Hz to 8kHz.
Otoacoustic emissions: Emissions to transient non-linear click stimulation were recorded at 80dBSPL. Spontaneous emissions were also recorded.
The tests were repeated between 5- 10 days in most subjects to check variability of emissions and tympanometry and audiometry.
An ENT physician examined each subject's ear and conducted the otoacoustic emissions testing and was trained for this purpose. The tympanometry and audiometry was conducted by a trained audiometrician working at the NOFER Institute of Occupational Medicine in Lodz.
Results and Analysis
198 subjects exposed to noise levels from 8595dBA for a mean of 12 + 6.6 years were tested, 104 with tinnitus and 94 without.
The mean age, pure tone average hearing loss across the frequencies (125Hz, 250Hz, 500Hz, 1kHz, 2kHz, 4kHz, 6kHz, 8kHz), transient emissions amplitude and variability are shown in [Table 2].
There were significant differences in the mean age, pure tone average, transient emissions amplitude and variability between the groups with and without tinnitus. There were no significant differences between the sessions in either group. Those with tinnitus had poorer hearing thresholds by an average of around 15dB. The transient emissions were also significantly reduced for the tinnitus group by on average around 2.6dB from those without tinnitus. There are a number of factors such as age, pure tone thresholds and tinnitus which may be responsible for the reduction in emissions.
There were no left/right ear differences within groups or across groups. Within groups, it was found that there were significant differences in the emissions of the order of 2dB between females and males. The females had higher emissions than males in both groups and those without tinnitus had even higher levels than those with tinnitus.
The spontaneous otoacoustic Emissions (SOAE) variability across subjects is shown in [Table 3]. Of the 94 subjects who had no tinnitus, 47 (50%) had spontaneous emissions present and of these 23 (48.9%) had spontaneous emissions, which varied from their original recording (shifted in frequency, absent or newly emerged in second test).
Thus 23 of the 94 (24.2%) of the subjects had variable spontaneous emissions. Of the 104 subjects with tinnitus, 76 (73.1%) had spontaneous emissions present and of these 70 (92%) and variable emissions on repeat testing. This provided an overall incidence of 70 from 104 (67.3%) with variable emissions compared with 24.2% in subjects without tinnitus.
There is a just under three-fold increase in the incidence of emission variability in tinnitus subjects than in those without tinnitus. The stable spontaneous emissions were considerably greater in those without tinnitus at 25.2% compared with 5.8% in subjects with tinnitus. [Figure 1] illustrates the stable, on-off, and shifted spontaneous emissions in a subject with tinnitus over two sessions. [Figure 2] illustrates the stable spontaneous emissions in subject with no tinnitus.
If only those in whom spontaneous emissions could be recorded are considered, almost 5 out of 10 had variable emissions in those without tinnitus, but over 9 out of 10 had variable emissions in those with tinnitus.
It appears that if a patient has spontaneous emissions which are stable, these are highly unlikely to be associated with the presence of tinnitus ( Calculations
Sensitivity= 92% (Proportion of people with tinnitus who have variable SOAE)
Specificity= 51% (Proportion of People who have no tinnitus and non-variable SOAE)
Positive Predictive Value = 92/141 = 65% (If SOAE variable what chances of patient having tinnitus)
Negative Predictive Value = 51/59= 86% (If SOAE stable what chances of patient NOT having tinnitus)
Likelihood Ratio (Positive) = 92/100/ 49/100
= 1.87 (odds of tinnitus given Variable SOAE)
Likelihood Ratio (Negative) = 8/100/51/100
= 0.156 (odds of no tinnitus given stable SOAE)
Sensitivity= 73% (Proportion of people with tinnitus who have SOAE)
Specificity= 50% (Proportion of People who have no tinnitus and no SOAE)
Positive Predictive Value = 73/123 = 59% (If SOAE present what chances of patient having tinnitus )
Negative Predictive Value = 50/77= 65% (If SOAE absent what chances of patient NOT having tinnitus )
Likelihood Ratio (Positive) = 73/100/ 50/100 = 1.46 (odds of tinnitus given Variable SOAE)
Likelihood Ratio (Negative) = 27/100/50/100 = 0.54 (odds of no tinnitus given stable SOAE)
The likelihood ratio of tinnitus being present given that the SOAE are present and variable is 1.87 and the likelihood is significantly reduced for no tinnitus given that SOAE are present and stable at 0.156. The results show a high sensitivity at 92% but a specificity of only 51%. The positive predictive value was calculated at 65% for those with variable SOAE having tinnitus and significantly higher at 86% negative predictive value for those with stable SOAE having no tinnitus.
It is clear that the prevalence of spontaneous emissions is higher than previously reported and can also be seen in subjects with islands of normal hearing. The spontaneous emissions are significantly more unstable on test repetition in subjects with tinnitus than in those without tinnitus. Although the instability in frequency is not restricted to those with tinnitus. Those subjects with high levels of spontaneous emissions tended to be more stable than those with weaker spontaneous emission levels. Stable spontaneous emissions were observed the least in subjects with tinnitus.
This study has clearly shown that the incidence of spontaneous emissions is higher in noise exposed group than previously observed and the stability from week to week is significantly lower in those with subjective tinnitus. The likelihood of an individual noise exposed worker having tinnitus and spontaneous emissions which are unstable is 7/10 and that without tinnitus having the same instability of spontaneous emissions is 2/10.
This study has clearly shown that it is possible to use the variability of spontaneous otoacoustic emissions as an objective indicator of the presence of subjective sensation of tinnitus in workers exposed to noise. The technique is clearly only viable in subjects with spontaneous emissions present.
In order to establish further the relationship between tinnitus and spontaneous emissions, it would be valuable to examine whether suppression of tinnitus by external stimulation alters the spontaneous emissions in a predictable way. Secondly it would also be worth exploring whether contralateral stimulation by sound alters spontaneous emissions and whether this has any impact on the perception of tinnitus. Auditory efferent system influences the cochlear micromechanics responsible for fine frequency selectivity. It is possible that some alteration of the efferent drive to the cochlear mechanics may be responsible for the tinnitus signal. Therefore an evaluation of the efferent system in subjects with and without tinnitus may provide further indication of the possible mechanisms responsible and an indication of the presence of tinnitus.
|1||Axelsson A, Ringdahl A. The occurrence and severity of tinnitus. In: Feldmann H, ed. Proceddings III International tinnitus Seminar, Munster. Karlsruhe: Harsch Verlag., 1987: 154-158.|
|2||Baskill JL, Coles RRA. Current studies on spontaneous emissions and tinnitus. In: Aran JM, Dauman R, eds. Tinnitus 91. Proceedings IV International Tinnitus Seminar, Bordeaux, Amsterdam/New York: Kuglar Publications, 1992: 79-83|
|3||Baskil JL, Coles RA. A two year study of SOAEs in tinnitus. In: Reich GE, Vernon JA, eds. Proceedings of the V International Tinnitus Seminar 1995, Portland, Oregan, USA. American Tinnitus Association, 1996a: 31-37|
|4||Bonfils P. Spontaneous otoacoustic emissions: Cliincial interest. Laryngoscope 189; 99: 752-756|
|5||Brix R, Denk DM, Ehrenberger K. Neurophysiological control in therapy of tinnitus with cochlear hearing loss. In: Reich GE, Vernon JA, eds. Proceedings of the V International Tinnitus Seminar 1995, Portland, Oregon, USA American Tinnitus Association, 1996: 101-105|
|6||Burns EM, Keefe DH. Intermittent tinnitus resulting from unstable otoacoustic emissions. In: Aran JM, Daumann R, eds. Tinnitus 91. Proceedings of the IV interntional Tinnitus Seminar, Bordeaux. Amsterdam/New York: Kuglar Publications, 1992: 82-93|
|7||Ceranic, B, Prasher, D, Luxon, L (1998a) Presence of tinnitus indicated by variable spontaneous otoacoustic emissions. Audiol. Neurootol. 3; 332-344|
|8||Ceranic, B, Prasher, D, Raglan, E, Luxon, L (1998b) Tinnitus after head injury: Evidence from otoacoustic emissions. J. Neurol. Neurosurg. Psychiatry 65(4); 523529|
|9||Coles RRA. Epidemiology tinnitus: (1) Prevalence and (2) Demographic and clinical feature. J Laryngol Otol Suppl. 9; 1984: (a) 7-15, (2) 195-202.|
|10||Coles RRA. Epidemiology, aetiology and classification. In: Reich GE, Vernon JA, eds. Proceedings of the V International Tinnitus Seminar 1995, Portland Organ, USA. American Tinnitus Association, 1996: 25-29|
|11||Cooper JC Jr. (1994) Tinnitus, subjective hearing loss and well-being. Health and Nutrition Examination Survey of 1971-75: Part II. J AM Ac Audiol 5: 37-43|
|12||Eggermont, JJ (1984) Tinnitus some thoughts about its origin. J. Laryngol. Otol (suppl.) 9; 31-37|
|13||Gold T.(1948) Hearing II. The physical basis for the action of the cochlea. Proc Roy Soc London, 135: 492-498|
|14||Hazell JWP. (1984) Spontaneous cochlear acoustic emissions and tinnitus. Clinical experience in tinnitus patients. J. Laryngol Otol; Suppl 9: 106-110.|
|15||Hazell, JWP (1987) A cochlear model of tinnitus. In Proceedings III International Tinnitus Seminar, Munster, 1987, Feldmann, H Ed. Karlsruhe: Harsh Verlag pp 121128|
|16||Hazell, JWP (1995) Models of tinnitus: generation, perception, clinical implications. In Vernon JA, Moller AR, eds. Mechanisma of tinnitus. Needham Heights, MA: Allyn and Bacon pp 57-72|
|17||Jasterboff PJ. (1990) Thantom auditory perception (tinnitus): Mechanisms of generation and perception. Neurosci Res 8: 221-254|
|18||Jasterboff PJ, Hazell JWP (1993) A neurophysiological approach to tinnitus: clinical implications. Br J. Audiol; 27: 7-17|
|19||Kemp DT. (1978) Stimulated acoustic emissions from within the human auditory system. J Acoust Soc Am 64: 1386-1391|
|20||Kemp DT. (1982) Cochlear echoes: Implications for noiseinduced hearing loss. In: Hamernik RP, Henderson D, Salvi R, eds. New perspectives of on noise-induced hearing loss. New York: Raven Press, 189-206.|
|21||Moller AR (1984) Pathophysiology of tinnitus Ann. Otlo. Rhinol. Laryngol. 93; 39-44|
|22||Moller AR, Moller MB, Yokota M. (1992) Some forms of tinnitus may involve the extralemniscal auditory pathway. Laryngoscope 109: 1165-1171|
|23||Norton S, Schmidt AR, Stover LJ. (1990) Tinnitus and otoacoustic emissions: Is there link? Ear Hear, 11: 159166|
|24||Penner MJ (1980)Two-tone forward masking patterns of tinnitus. J Speech Hear Res 23: 779-786|
|25||Penner MJ, Burns E. (1987a) Dissociation of spontaneous acoustic emissions and tinnitus J. Speech Hear Res 30: 369-403|
|26||Penner MJ, Burns E. (1987b) Five empirical tests for relation between spontaneous acoustic emissions and tinnitus. In: Feldmann H, ed. Proceedings III International Tinnitus Seminar, Munster. Karlsruhe: Harsh Verlag, 82-85|
|27||Penner MJ. (1988) Audible and annoying spontaneous otoacoustic emissions. Arch Otolaryngol Head Neck Surg 114: 150 - 153|
|28||Penner MJ. (1989) Empirical tests demonstrating two coexisting sources of tinnitus: a case study. J Speech Hear Res 32: 458-462|
|29||Penner MJ. (1990) An estimate of the prevalence of tinnitus cuased by spontaenous otoacoustic emissions. Arch Otolaryngol Head Neck Surg 116: 418-423|
|30||Penner MJ. (1992) Linking spontaneous acoustic emissions and tinnitus. Br J Audiol 26: 115-123|
|31||Penner MJ, Coles RR. (1992) Indications for aspirin as a palliative for tinnitus cuased by spontaneous acoustic emissions: A case study. Br J Audiol 26 92-96|
|32||Plinkert PK, Gitter AH, Zenner HP. (1990) Tinnitus assoicated with spontaneous acoustic emissions. Acta Otolaryngol 110: 342-347|
|33||Prasher, D, Ryan, S, Luxon, L (1994). Contralateral suppression of transiently evoked otoacoustic emissions and neuro-otology. Br. J. Audiol 28:247-254|
|34||Prasher, D, Tun, T, Brookes, G, Luxon, L. (1995) Mechanisms of hearing loss in acoustic neuroma: An otoacoustic emission study. Acta Otolaryngol (Stockh) 115; 375-381|
|35||Probst R, Lonsbury-Martin BL, Martin BK, Coats AC. (1987) Otoacoustic emissions in ears with hearing loss. Am J. Otolaryngol ; 8: 73-80|
|36||Pujol R. Puel JL, Gervais d'Aladin C, Eybalin M. (1993) Pathophysiology of the glutamergic synapses in the cochlea. Acta Otolaryngol (Stockh) 113: 330-334|
|37||Quaranta A, Assennato G, Sallustio V. (1996) Epidemiology of hearing problems among adults in Italy. Scand Audiol Suppl 42: 7-11.|
|38||Rajan R, Irvine DRF, Claford MB, Wise LZ. (1992) Effects of frequency-specific losses in cochlear neural activity on the processing and representation of frequency in primary auditory cortex. In: Dancer Al, Henderson D, Salvi RJ, Hamernik RP, eds. Noise induced hearing loss. St. Louis: Mosby Year Book, 119-129|
|39||Salvi RJ, Powers NL, Saunders SS, Boettcher FA, Clock A (1992). Enhancement of evoked response amplitude and single unit activity after noise exposure. In: Dancer AL, Henderson D, Salvi Rj, Hamernick RP, eds. Noise induced hearing loss. St. Louis: Mosby Year Book, 156-171|
|40||Schwaber MK, Garraghty PE, Kaas JH. (1993) Neuroplasticity of the adult primate audiotry cortex following cochlear hearing loss. Am J Otol, 3: 252-258|
|41||Tonndorf J. (1987). The analogy between tinnitus and pain: A suggestion for physiological basis of tinnitus. Hear Res. 28: 271-275.|
|42||Tyler RS, Conrad-Armes D. (1982) Spontaneous acoustic emissions and sensory-neural tinnitus. Br. J. Audiol, 16: 193-194|
|43||Wilson, JP. (1980) Evidence for a Cochlear origin for acoustic re-emissions, threshold fine -structure and tonal tinnitus. Hear Res 233-252|
|44||Wilson, JP, Sutton G.J. (1981) Acoustic correlates of tonal tinnitus. In: Evered D, Lawrenson G, eds. Tinnitus (CIBA Foundation Symposium). London: Pitman Books Ltd. 82107.|
|45||Zurek PM. (1981) Spontaneous narrowband acoustic signals emitted from human eares. J. Acoust Soc Am 69: 514-523|
|46||Zurek PM, Clark WW. (1981) Spontaneous narrowband acoustic signals emitted by chinchilla ears after noise exposure. J Acoust Soc Am. 70: 446-450.|
|47||Zwicker E. (1987a) Masking in normal ears - psychoacoustical facts and physiological correlates. In: Feldmann H, ed. Proceedings III International Tinnitus Seminar, Munster. Karlsruhe: Harsch Verlag, 214-223.|
|48||Zwicker E. (1987b) Objective otoacoustic emissions and their uncorrelation in tinnitus. In: Feldmann H, ed. Proceedings III International Tinnitus Seminar, Munster. Karlsruhe: Harsch Verlag, pp. 75-81.|