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Electrically Evoked Brainstem Responses in Cochlear Implant Recipients
Abstract
Electrical stimulation of the auditory nerve in the profoundly deaf population through implanted cochlear prostheses has increased the need for reliable electrophysiologic assessment tools. We have recorded electrically evoked brainstem responses (EABRs) in 21 subjects who have received a 3M/House cochlear implant. Recordings have been made, both intraoperatively and postoperatively, in the laboratory setting. The recording technique, methods of stimulus artifact suppression, and results of our measurements are described. Clinical applications of this technology are suggested.
... Initial EABR eIII and eV mean latencies (2.4, 4.4 msec, respectively) and eIII-eV interwave mean latency (2.0 msec) in children were longer than those reported in implanted adults (Abbas & Brown, 1988;Abbas & Brown, 1991;Gallego, Frachet, Micheyl, Truy, & Collet, 1998;Gallego et al., 1999;Miyamoto & Brown, 1987;Shallop, Beiter, Goin, & Mischke, 1990 ...
... With consistent electrical stimulation, changes in the brain stem were realized as reductions in neural conduction time and increases in response amplitudes. Absolute wave latencies for waves eN1, eIII, and eV significantly decreased within several months of implant use becoming more similar to reported adult EABR values (Fig. 6) (Abbas & Brown, 1988;Abbas & Brown, 1991;Gallego et al., 1998;Gallego et al., 1999;Miyamoto & Brown, 1987;Shallop et al., 1990;Truy et al., 1998;van den Honert & Stypulkowski, 1986). Figure 8 shows that wave amplitudes increased significantly for eN1 and eV (increasing without statistical significance for eIII). ...
... Direct comparisons between ABR and EABR parameters are difficult because it is possible that the two responses reflect different neural generators. For example, EABR data reported from implanted adults indicate that wave eIII occurs at approximately 2.0 msec (Abbas & Brown, 1988;Abbas & Brown, 1991;Gallego et al., 1998;Gallego et al., 1999;Miyamoto & Brown, 1987;Shallop et al., 1990;Truy et al., 1998;van den Honert & Stypulkowski, 1986). Given that normal adult ABRs show a I-III interwave latency of approximately 2.1-2.2 msec (Beiser, Himelfarb, Gold, & Shanon, 1985;Eggermont & Salamy, 1988), the EABR eI-eIII measure in implanted adults is shorter than normal. ...
1) To determine if a period of early auditory deprivation influences neural activity patterns as revealed by human auditory brain stem potentials evoked by electrical stimulation from a cochlear implant. 2) To examine the potential for plasticity in the human auditory brain stem. Specifically, we asked if electrically evoked auditory potentials from the auditory nerve and brain stem in children show evidence of development as a result of implant use. 3) To assess whether a sensitive or critical period exists in auditory brain stem development. Specifically, is there an age of implantation after which there are no longer developmental changes in auditory brain stem activity as revealed by electrically evoked potentials?
The electrically evoked compound potential of the auditory nerve (ECAP) and the electrically evoked auditory brain stem response (EABR) were recorded repeatedly during the first year of implant use in each of 50 children. The children all had pre- or peri-lingual onset of severe to profound sensorineural hearing loss and received their implants at ages ranging from 12 mo to 17 yr. All children received Nucleus cochlear implant devices. All children were in therapy and in school programs that emphasized listening and required the children to wear their implants consistently.
Initial stimulation from the cochlear implant evoked clear responses from the auditory nerve and auditory brain stem in most children. There was no correlation between minimum latency, maximum amplitude, or slope of amplitude growth of initial responses with age at implantation for ECAP eN1, EABR eIII and eV components (p > 0.05). During the first year of implant use, minimum latency of these waves significantly decreased (p < 0.01, p < 0.0001, p < 0.0001, respectively). Neural conduction time, measured using the interwave latency of ECAP eN1-EABR eIII for lower brain stem and EABR eIII-eV for upper brain stem, decreased during the period of 6 to 12 mo of cochlear implant use (p < 0.01 (lower), p < 0.0001(upper)). The ECAP wave eN1 and the EABR wave eV showed significant increases in amplitude during time of implant use (p < 0.05 and p < 0.01, respectively). There were no correlations between the rate of interwave latency decrease and the rate of amplitude increases and the age at which children underwent implantation (p < 0.05).
Activity in the auditory pathways to the level of the midbrain can be evoked by acute stimulation from a cochlear implant. EABR measures are not influenced by any period of auditory deprivation. Auditory development proceeds once the implant is activated and involves improvements in neural conduction velocity and neural synchrony. Underlying mechanisms likely include improvements in synaptic efficacy and possibly increased myelination. The developmental plasticity that we have shown in the human auditory brain stem does not appear from EABR data to be limited by a critical period during childhood.
... This latency value is delayed by almost three standard deviations and approximately 1 ms when compared with the normative EABR data. 27 This increase in latency occurs between waves I and III as the interwave latency wave III to V is normal. This would correlate with a lesion located on the cochlear nerve, which would affect nerve conduction between sites responsible for the generation of waves I and III of the ABR. ...
... The EABR, however, did not return despite waiting for 5 minutes. Before the sudden decrease in wave V amplitude, the morphology of wave V was widened (see recordings [25][26][27] in ►Fig. 4), and this may have been a more sensitive indicator of impending cochlear nerve damage. ...
Objectives A decision on whether to insert a cochlear implant can be made in neurofibromatosis 2 (NF2) if there is objective evidence of cochlear nerve (CN) function post vestibular schwannoma (VS) excision. We aimed to develop intraoperative CN monitoring to help in this decision.
Design We describe the intraoperative monitoring of a patient with NF2 and our stimulating and recording set up. A novel test electrode is used to stimulate the CN electrically.
Setting This study was set at a tertiary referral center for skull base pathology.
Main outcome measure Preserved auditory brainstem responses leading to cochlear implantation.
Results Electrical auditory brainstem response (EABR) waveforms will be displayed from different stages of the operation. A cochlear implant was inserted at the same sitting based on the EABR.
Conclusion Electrically evoked CN monitoring can provide objective evidence of CN function after VS excision and aid in the decision-making process of hearing rehabilitation in patients who will be rendered deaf.
... Even though the acoustically evoked compound action potential (CAP) has been widely used in basic and clinical studies for more than six decades (Goldstein and Kiang, 1958), the feasibility of measuring the eCAP in animals or human listeners was not established until late 1980s (van de Honert and Stypulkowski, 1986;Game et al., 1987;Miyamoto and Brown, 1987;Abbas and Brown, 1988). The delay is primarily due to the lack of technique for recognizing and minimizing contamination of stimulus artifact on the recorded response. ...
The electrically evoked compound action potential (eCAP) represents the synchronous firing of a population of electrically stimulated auditory nerve fibers. It can be directly recorded on a surgically exposed nerve trunk in animals or from an intra-cochlear electrode of a cochlear implant. In the past two decades, the eCAP has been widely recorded in both animals and clinical patient populations using different testing paradigms. This paper provides an overview of recording methodologies and response characteristics of the eCAP, as well as its potential applications in research and clinical situations. Relevant studies are reviewed and implications for clinicians are discussed.
... More recently, electrophysiological evidence of binaural interaction has also been revealed in bilateral CI users [13,17,22]. These responses evoked by direct stimulation of cochlear-implant electrodes rather than acoustical stimulation have been termed EABR, and exhibit distinguishing characteristics from ABRs [18,21], namely earlier peak latencies and higher peak amplitudes [23][24][25]. A pronounced electrically evoked BIC, consisting of a negative peak around 3.6 ms followed by a positive peak near 4.4 ms was shown [16], being attributable to the fact that electrical pulses stimulated fibers of the auditory nerve synchronously. ...
Bilateral cochlear implants (BiCIs) have succeeded in improving the spatial hearing performance of bilateral CI users, albeit with considerable variability across implantees. Limited success can be caused by an interaural mismatch of the place-of-stimulation that arises from electrode arrays being inserted at different depths in each cochlea. In comparison to subjective pairing methods such as pitch matching, one promising objective measure based on electrically evoked auditory brainstem responses (EABR), the binaural interaction component (BIC), could be used to optimize the interaural electrode pairing (IEP) in BiCIs. Matched interaural electrodes are expected to facilitate binaural functions such as binaural fusion, localization, or detection of signals in noise. An IEP system, currently under development for clinical research, is proposed. The system offers subjective and objective IEP methods for BiCI: a psychoacoustic test module for pitch ranking and interaural pulse time difference (IPTD) sensitivity, and a binaural and monaural EABR recording module to derive the BIC. Psychoacoustic and IEP measures from two implantees are presented.
... A number of previous studies of adult EABR suggested similar eIII-eV intervals compared to normal III-V interlatencies [van den Honert and Stypulkowski, 1986;Miyamoto and Brown, 1987;Gallego et al., 1998;Truy et al., 1998] and these similarities were used to suggest that the ABR and EABR refl ected activity from the same auditory brainstem generators. Interestingly, eIII-eV latencies were fairly consistent between these studies (approximately 1.85 ms) despite differences in device (single vs. multi-electrode implants), differences in stimulus presentation rates (10-60 Hz), and differences in intensity (near electrophysiologic threshold -uncomfortable loudness limits). ...
Central auditory responses to electrical stimulation from a cochlear implant were studied in 75 pre-lingually deafened children and 11 adults. Electrically evoked auditory brainstem response (EABR) latencies significantly decreased with duration of cochlear implant use and were not significantly affected by the age at implant activation. Significant decreases in early latency waves and interwaves occurred within the first 1-2 months of implant use, whereas longer term changes (6-12 months) were found for eV and eIII-eV, which measure activity in the more rostral brainstem. Comparisons to acoustically evoked auditory brainstem response (ABR) in children with normal hearing suggested shorter interwave EABR latencies, reflecting either distinct neural generators or increased neural synchrony, but similar rates of change in the later latency eV and eIII-eV with time in sound. In sum, normal-like development of the rostral auditory brainstem is promoted by cochlear implant use in children of a wide range of ages.
The nondeafened guinea pig model was utilized in this study to assess the functional and morphologic effects of cochlear implantation and electrical stimulation. Auditory brainstem responses (ABRs) were recorded prior to and following intrascalar implantation of a 3M-House cochlear electrode (n = 41 ears), as well as after electrical stimulation (n = 23 ears). The experimental population was divided into the following groups according to implantation and stimulation parameters: 200 microA for 3 hours (group I); 200 microA for 24 hours (group II); 400 microA for 3 hours (group III); implanted, but not stimulated (group IV); and nonimplanted, not stimulated ears (group V). Of those cochleae that sustained the trauma of implantation, 32 percent had no detectable ABR to 110 dB SPL clicks, while only 7 percent additionally failed to respond to 130 dB SPL clicks. No significant difference (one-way ANOVA with repeated measures at the 95 percent confidence limit) could be detected when comparing those ears that retained ABRs according to experimental grouping. Morphologic analysis was performed on 29 cochleae. Spiral ganglion "packing densities" were not found to be significantly different among the groups (ANOVA). The status of the organ of Corti was significantly better in groups II and V in comparison to the other groups (Kruskal-Wallis test with pairwise comparisons, p less than 0.05); there was no discernible dose-response relationship. Morphologic and electrophysiologic changes correlated with insertion trauma and infection rather than with electrical stimulation at the levels tested in this study.(ABSTRACT TRUNCATED AT 250 WORDS)
Ossification of the cochlea following meningitis presents a surgical challenge. Electrode mapping, especially in the young child, is difficult given the uncertainty of electrode contact with viable neural elements. This paper reviews surgical technique and the use of auditory brainstem responses to map the electrodes.
A 4-year-old child deafened by meningitis at age 20 months had bilateral cochlear ossification by computed tomography. At surgery, a canal wall-down mastoidectomy and closure of the ear canal were performed. A trough around the modiolus was drilled, and the electrode array was placed in it. Post-operatively, the patient gave aversive or no responses to electrode stimulation. To assess electrode function, auditory brainstem responses to individual electrode activation were obtained under general anesthesia. Functioning electrodes could thus be selected for mapping. The patient now responds well to sound.
The electrically evoked brainstem response (EABR) was measured in cochlear implant users who had received either the Ineraid multichannel implant or the Nucleus multichannel implant. Although both implants use a multi-electrode array, they are different in a number of ways. In the Ineraid system the electrodes can be accessed directly through a percutaneous plug and stimulation is generally on four different intracochlear electrodes relative to a common ground outside the cochlea. In the Nucleus implant stimulation is accomplished via an internal coil and stimulation is bipolar between pairs along the 22 electrode array. The ABR waveforms were similar for both groups of subjects, consisting of a series of 3 or 4 positive peaks at the highest levels of stimulation. Using the normal stimulation mode (bipolar for Nucleus and monopolar for Ineraid), users of both devices demonstrated an increase in response amplitude and a decrease in response latency with increases in current level. The threshold of response tended to be higher and growth of the response with level tended to be more gradual for Nucleus users than for Ineraid users. However, with bipolar stimulation for both implant types, when the stimulating electrodes were closely spaced the threshold of response was higher and the growth of amplitude with level was more gradual than the case where the electrodes were separated further. When bipolar stimulation and similar electrode spacing was used, the response growth and threshold were similar for both implant types. Results from neither device showed a strong correlation with performance on word recognition tests.
Two cases demonstrating the effects of myogenic artifact on the electrical auditory brainstem response (EABR) when using a promontory stimulation site are presented. Intensity-response functions were obtained in the unparalyzed condition, then repeated after infusion of a neuromuscular paralyzing agent. In both cases, the myogenic response was observed at lower stimulus intensities than the EABR components. As intensity increased, the myogenic responses grew at extremely rapid rates and made any subsequent identification of auditory responses virtually impossible. To alleviate the adverse influence of myogenic components, general anesthesia and a paralyzing agent must be incorporated into the test protocol when acquiring the EABR using a promontory site of stimulation.
Binaural interaction was demonstrated in electrically evoked brainstem responses (EBRs) of a bilaterally implanted patient. A clear binaural difference waveform (BD), consisting of a negative peak near 3.6 ms followed by a positive peak near 4.4 ms, was found by subtracting the recordings with diotic stimulation from the sum of the recordings with monotic stimulation. These results are consistent with those reported for normal subjects and suggest that neural processing in this patient might resemble those ordinarily used in binaural hearing. They strengthen the argument that EBRs in cochlear implant patients do result from activity in auditory brainstem neurons and suggest a method for aligning the positions of the intracochlear electrodes.
Auditory brainstem responses evoked by electrical stimulation with a Nucleus/Cochlear implant can be measured if care is taken to prevent stimulus artefacts. A simple procedure is described which relies upon a passive LCR filter to prevent the radiofrequency carrier from entering the input of the recording amplifier. The filter simply prevents saturation of the amplifier by the carrier.
The electrically evoked brainstem potential was measured in cochlear implant patients with Symbion multichannel electrode system. In the first experiment, electrodes within the implant were stimulated individually and the responses and sensitivity across electrodes and across subjects were evaluated. The typical response waveform consisted of a series of three peaks, the most prominent occurring at approximately 4 ms after stimulus onset. The amplitude of the largest peak typically showed an orderly increase with increasing current level while latency changes were relatively small. In the second experiment, two electrodes were stimulated simultaneously in order to evaluate the relative independence of the neural populations being stimulated by the different electrode pairs. The responses were compared when two electrode pairs were stimulated simultaneously with current pulses in phase and when the same electrodes were stimulated with current pulses inverted relative to each other. Both stimulation conditions showed similar growth in response amplitude with level but different sensitivity. The differences in sensitivity between these two conditions may be indicative of the degree of overlap in the stimulated neural populations.
The electrically elicited auditory brain-stem response (EABR) has been proposed as a tool for use in cochlear implant device setting. To systematically examine the relationships of psychophysical perceptions and EABRs, implant users underwent a series of comparative measurements. The characteristics of the EABR were assessed for their predictive value in determining the subjective measures needed to set the implant device.
Characteristics of the EABR and various perceptual measures in a group of cochlear implant users served as compared variables in a correlational study.
The study was carried out in the audiology clinic of a university hospital. The audiology clinic maintained a fully equipped evoked potential laboratory, and was part of an otolaryngology department that supported a cochlear implant program.
The subjects consisted of 10 consecutively selected postlinguistically deafened adult multichannel cochlear implant users.
Morphology, latency, and amplitude measures of the EABR recordings were compared with behavioral perceptions of threshold, most comfortable and uncomfortable loudness levels.
Perceptual measures of threshold were found to be significantly related to the threshold of the EABR across subjects and electrode position. Simple linear regression analysis was used to measure the degree of the relationship. An r value of 0.89 attests to a significant relationship. The EABR wave latencies and amplitudes were found to have no significant relationship to any of the perceptual measures examined.
Although EABR cannot replace behavioral measurements for device setting, in difficult cases EABR thresholds may be used as a starting point from which to estimate settings for the device.
The electrically evoked auditory brainstem response (EABR) was recorded by direct electrical stimulation of the cochlear nerve in 8 acoustic neuroma patients. The EABR by electrical stimulation of the cochlear nerve at the fundus of the internal auditory canal was almost similar to those previously reported from cochlear implant patients in waveform morphology and wave latencies. However, the wave corresponding to wave II in human auditory ABR was not recorded in the EABRs by stimulation of the distal part of the intracranial cochlear nerve. These results suggest that the cochlear nucleus does not contribute to the generation of wave II in ABR.
The purpose of this study was to determine stimulation and recording parameters that maximize differences in evoked responses recorded between the cochlear nerve and the surrounding tissues. Click-evoked potentials were obtained using monopolar and bipolar recording electrodes placed directly on the exposed eighth nerve of anesthetized cats. Responses were compared as stimulus intensity, electrode location, and bipolar electrode orientation and interelectrode spacing were systematically varied. Wave amplitudes increased monotonically with intensity for both monopolar and bipolar configurations, but bipolar configurations exhibited greater selectivity in differentiating cochlear from vestibular subdivisions. The optimal stimulus intensity was 70 to 80 dB peak sound pressure level (pSPL). Monopolar recordings were often confounded by activity originating at remote sites, typically the cochlear nucleus and (for recording sites on the vestibular nerve) the cochlear nerve. Bipolar response amplitudes increased with interelectrode spacing and were largest when electrodes were oriented parallel to the long axis of the nerve. Extrapolation of empirical data indicated that amplitudes of bipolar responses would be maximal at an electrode separation of 7.5 mm. Cochlear nerve conduction velocity, calculated from wave latencies at each of the two monopolar electrodes, was 11.6 +/- 1.6 m/sec.
Brain stem potentials were recorded from scalp electrode to biphasic square wave electrical stimulation of implanted electrodes in the cochlea of three patients. Reliable potentials could be recorded that appeared 1.5 to 2.0 msec prior to the customary acoustically-evoked brain stem potentials. The effects of variations in electrical stimulus parameters of rate and intensity were measured. Brain stem potentials can provide objective indices of the effectiveness of electrical stimulation of the cochlea in man.
A series of experiments was performed to study electrically evoked potentials as indicators of subject response to cochlear implantation. 1. Brain stem evoked responses to electrical stimulation were compared to those obtained by acoustic stimulation in guinea pigs. The response pattern was similar and was independent of the site of placement of the stimulus electrode (cochlear base or apex) or of the extracochlear ground electrode (eustachian tube or temporalis muscle) when evoked electrically. 2. Electrically evoked middle latency responses were recorded and compared to subjective behavioral thresholds in patients who had received a single channel cochlear implant (House-Urban). The behavioral responses to the same stimuli were similar. 3. Electrically evoked auditory brain stem responses were studied in single channel cochlear implant subjects (3M/House). When evoked electrically, potential latencies were shorter and interpeak intervals narrower than acoustically evoked potentials.
Electrically evoked auditory brainstem response (EABR) recordings were made from 38 humans implanted with one of three cochlear prostheses, and from 25 cats. Recognizable auditory potentials were identified in 27 of the profoundly deaf implanted subjects. In both cats and humans EABR waveform morphology and magnitude were independent of electrode configuration and paralleled those of the normal acoustic ABR, but with reduced absolute latencies. EABR recordings are highly susceptible to contamination by stimulus artifact and by elicited non-auditory potentials. Latency, morphology, and magnitude criteria are proposed for identification and analysis of EABR components.
Fifteen profoundly deaf patients under the age of 18 years have received a 3M/House cochlear implant. The surgical procedure employed is essentially the same as that used in adults with a few modifications to accommodate for the smaller dimensions of the mastoid process and the thinness of the scalp and temporal squama. Pediatric subjects receive timing and intensity information at similar thresholds as adults implanted with this device which contributes to improvement in speech production to various degrees. All subject groups demonstrated significant language delays as a result of their profound hearing losses. Postimplantation, more growth was seen in receptive than in expressive language skills. However, the growth observed did not exceed that expected in profoundly deaf children as reported in the literature. Language growth as a result of the cochlear implant alone is yet to be documented in our patients.
Nerve survival estimates in totally deaf ears of cats and humans can be easily obtained by auditory brainstem responses to electrical stimulation at the round window. In humans, electrically induced auditory brainstem responses require considerably more current than concurrently observed perceptual thresholds and "maximum loudnesses," and there is much variability from patient to patient. In cats, in which we also compared efficacy of stimulation sites, preliminary data analysis suggests that the scala tympani is clearly much more efficient than the round window, and the round window better than the promontory in ears with large populations of ganglion cells. In ears with no or nearly no ganglion cells, scala tympani and round window stimulations are about equal.
The decision to implant cochlear prostheses in children came after positive findings with deaf adults and the belief that the benefits of receiving sound far outweigh the potential risks involved. As of December 1981, 12 profoundly deaf children have received the single-electrode cochlear implant. Their ages range from 3.5 to 17 years. Test results are consistent with those of adults. Mean thresholds across the frequency range fall between 59-64 dB SPL. With the implant, these children can perform specific timing and intensity differentiations which could not be done with hearing aids. Their voices are quieter and more modulated, and the children are not quite as noisy with objects in the environment (eg, do not slam doors any more). This preliminary data demonstrates that implanting subjects under the age of 18 years is feasible.
Introducing sound to the prelingually deaf adult presents a special challenge to those concerned with the rehabilitation of the deaf utilizing the cochlear implant. Twelve subjects with an early loss have undergone implant surgery and have been fitted with external stimulator devices. Eight of the 12 subjects are considered successful users. Electrical thresholds are comparable to those for the postlingually deaf. However, the prelingual subjects initially have a reduced tolerance for sound and often react differently than the postlinguals. The prelinguals do not always respond to the sensation as sound, but rather as a feeling or vibration in the head. However, like the postlinguals, the prelingually deaf report being able to respond to attention-getting sounds, such as horn-honks and their names being called; and voice quality changes have been noted. These subjects find music particularly enjoyable through the implant. In addition, they have reported feeling more independent, more social, and even less lonely.
The cochlear implant: an auditory prosthesis for the profoundly deaf child
- Berliner KI