Ups and Downs in 75 Years of Electrocochleography

Jos J Eggermont, Jos J Eggermont

Abstract

Before 1964, electrocochleography (ECochG) was a surgical procedure carried out in the operating theatre. Currently, the newest application is also an intra-operative one, often carried out in conjunction with cochlear implant surgery. Starting in 1967, the recording methods became either minimal- or not-invasive, i.e., trans-tympanic (TT) or extra tympanic (ET), and included extensive studies of the arguments pro and con. I will review several valuable applications of ECochG, from a historical point of view, but covering all 75 years if applicable. The main topics will be: (1) comparing human and animal cochlear electrophysiology; (2) the use in objective audiometry involving tone pip stimulation-currently mostly pre cochlear implantation but otherwise replaced by auditory brainstem response (ABR) recordings; (3) attempts to diagnose Ménière's disease and the role of the summating potential (SP); (4) early use in diagnosing vestibular schwannomas-now taken over by ABR screening and MRI confirmation; (5) relating human electrophysiology to the effects of genes as in auditory neuropathy; and (6) intracochlear recording using the cochlear implant electrodes. The last two applications are the most recently added ones. The "historical aspects" of this review article will highlight the founding years prior to 1980 when relevant. A survey of articles on Pubmed shows several ups and downs in the clinical interest as reflected in the publication counts over the last 75 years.

Keywords: Ménière’s disease; auditory nerve; auditory neuropathy; cochlear implants; cochlear microphonic; compound action potential; summating potential; vestibular schwannoma.

Figures

Figure 1
Figure 1
Ups and Downs in the number of publications on Electrocochleography (ECochG), overall and applied to Ménière’s disease. I tabulated all ECochG articles between 1941 and present that I could find in PubMed and added those from a 1976 conference proceeding (Ruben et al., 1976), amounting to 358 publications covering 75 years. I grouped them in periods of 6 years, because that bracketed the early minimum-intervention recording period from 1967–1972. The first 25 years before that I grouped together. The last period ending July 2016 covers 6.5 years.
Figure 2
Figure 2
Transition of a negative to a positive summating potential (SP+) with increase in tone burst frequency. In some ears, a quite sudden change in the sign of the SP may be observed. In this example, a change occurs between 4750 Hz and 5175 Hz. This type of transition from SP− to SP+ typically occurs between 4 kHz and 8 kHz. From Eggermont (1976c).
Figure 3
Figure 3
(A,B) SP and compound action potential (CAP) waveforms as a function of the interstimulus interval (ISI). The SP, being a pre-synaptic potential, does not show the phenomenon of adaptation as the CAP does. When the ISI value is lowered the CAP amplitude decreases but the SP amplitude remains constant. Panel (A) shows at an ISI of 4 ms, only the SP− remains and closely resembles the stimulus envelope. From Eggermont and Odenthal (1974a). Panel (B) shows a combination of SP+ and SP− in one recording. In ears showing a transition from SP− to SP+ as described in Figure 6, for high frequencies a quite peculiar phenomenon may be observed. It appears as an SP+ followed after some latency by a smaller SP− thus forming an early positive peak, which is persistent to low intensity levels. From Eggermont (1976c).
Figure 4
Figure 4
ECochG recordings obtained from three representative ears showing normal CAP threshold, elevated CAP threshold and the absence of neural response at maximum stimulation intensity (clicks, 120 dB p.e. SPL). CAP and cochlear microphonics (CM) traces were obtained by the classic procedure of averaging recordings to condensation and rarefaction clicks. Note the ringing of the click-evoked CM. From Santarelli et al. (2006).
Figure 5
Figure 5
Human cochlear APs as recorded in response to tone bursts (envelope shown near abscissa) between 95 dB HL and 15 dB HL. In these series of APs, the sudden jump in the latency-intensity curves is illustrated. Note the appearance of a double-peaked N1/N2 complex at 65 dB HL and the difference between the latencies of the first negative wave at 65 dB HL and 55 dB HL. The scaling changes with intensity as indicated. From Eggermont (1976c).
Figure 6
Figure 6
Waveforms of CAPs in recruiting ears. These waveforms may be either of the broad type (A) or of the biphasic type (B). The diphasic type in this case was recorded for a cochlea with hearing loss to asphyxia at birth. The absence of a bimodal N1 complex and the consistent short latencies along with an abrupt amplitude decrease draw a distinction between normal (see Figure 5) and recruiting ears. The broad type was recorded in a Ménière ear. There was an interval of about a year between the times (dates in A top right) when the two sets of waveforms were recorded for the Ménière ear; quite dramatic changes are noted in the about 1 year time difference. From Eggermont (1976c).
Figure 7
Figure 7
Input-output curves for recruiting ears in response to 2000 Hz tone burst stimulation. For six recruiting ears, the input-output curves are drawn. The data for the three series of CAPs shown in the former figure are indicated by triangles (the diphasic type) and open and filled circles (the Ménière ear). A common phenomenon for all curves is that the slope for amplitude values below, e.g., 1.5 μV is essentially the same and much larger than that found in normal ears. The median input-output curve is based upon data for 20 normal ears. From Eggermont (1977).
Figure 8
Figure 8
(A,B) Adaptation and forward masking of the CAP. (A) The amplitude of the CAP depends on the ISI. For six normal human cochleas, the relative decrease in amplitude is shown and compared to the mean for guinea pigs at a comparable stimulus level and shows a clear difference. The 50% relative amplitude point is found at a time about four times longer in humans than in the guinea pig. ISI, inter-stimulus interval. From Eggermont and Odenthal (1974a). (B) The relative CAP amplitude value in a forward-masking experiment as a function of the delay between the end of the white-noise masker and the tone-burst. In this experiment a 400 ms white-noise masker precedes a shore tone-burst. The CAP amplitude in response to this tone-burst depends on both the time (6t) after the masker and the intensity ratio between masker and tone-burst. In the human it takes about 1 s for full recovery from masking; in the guinea pig this value is about four times smaller. Δt, post-masker delay. From Eggermont and Odenthal (1974b).
Figure 9
Figure 9
High-pass noise masking and the derivation of narrow band APs (NAPs) in humans. The upper two traces show the whole nerve CAP for a normal ear in response to a 90 dB p.e. SPL click and reflect the situation where just complete masking by wide-band noise occurs. On the left hand side the effect of high-passing the noise at successively higher cut-off frequencies can be seen. Subtraction of two subsequent CAP’s results in the set of narrow-band CAP’s in the right-hand side. From Eggermont (1979c).
Figure 10
Figure 10
Narrow band response parameters as a function of central frequency (CF). For clicks of 70, 80, and 90 dB p.e. SPL, narrow band amplitudes are shown as a function of distance from the stapes; it is observed that for the highest intensity the amplitudes decrease by about 3 dB/octave. Lowering the click intensity results in a decrease for contributions from both the apical and basal part of the cochlea, while the central part still contributes the same. The latency data show an exponential dependency on the distance from the stapes, and a definite effect of stimulus intensity thereupon is noted. From Eggermont (1976c).
Figure 11
Figure 11
CAP and NAP waveforms for a normal ear, a Ménière’s ear and a neuroma ear. As has been observed consistently in many cases there is a typical Ménière’s and acoustic neuroma type of AP waveform which is very distinct from normal. The distinction between both pathologies on basis of the CAP-waveform, however, in general presents some difficulties. A narrow-band analysis shows that the individual NAP-waveforms are different for all three hearing states, which may be of help in further diagnosis but also provides an insight in the location of the disturbance. From Eggermont (1976a).
Figure 12
Figure 12
Relationship between objective and subjective hearing thresholds. Peripheral and central (subjective) measurements are similar except for a few ears. This similarity indicates that 8th nerve tumors usually produce a peripheral hearing loss (Eggermont et al., 1980).
Figure 13
Figure 13
(A) CAP waveforms in response to 2 kHz tone burst stimulation in three ears with acoustic neurinoma. Depending on the individual case as well as on stimulus intensity, broad characteristic waveforms or nearly normal CAPs can be found. It appears that the CAP waveform is not consistently abnormal in acoustic neurinoma ears. (B) Narrow band AP waveforms in acoustic neurinoma ears. From dominantly monophasic NAPs in the left series to strictly biphasic narrow band responses in the right series, reminding us of a sensorineural hearing loss, the relationship to the CAP waveforrn is clear. From Eggermont et al. (1980).
Figure 14
Figure 14
(A) CAP width-latency data for 2 kHz tone burst stimulation for the tumor ears. About 20% of the points are well outside the normal range. (B) SP amplitudes for 85 dB HL tone bursts as a function of the CAP threshold. Up to 50 dB HL thresholds, the SP amplitude appears stable; for higher hearing losses, the SP amplitude decreases and often the SP is absent. This trend is also observed in a large group of ears with Ménière’s disease whose median value is indicated. Moreover, the median values of tumor ears are smaller by a factor of at least 2. From Eggermont et al. (1980).
Figure 15
Figure 15
(A) Comparison between the SP–CAP potentials recorded from one subject with OTOF mutations and one control. The curves for the OTOF subject are superimposed on the recordings obtained from one control at intensities up to 120 dB p.e. SPL to highlight the similarities of the SP component between controls and patients with OTOF mutations. Open circles and triangles refer to the CAP and SP peaks, respectively. From Santarelli et al. (2009). (B) ECochG waveforms obtained after CM cancellation from two representative OPA1 patients are superimposed on the corresponding responses recorded from one normal hearing control and from one hearing-impaired child with cochlear hearing loss (Cochlear HL) at decreasing stimulus intensity. From Santarelli et al. (2015).

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