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Acoustically and electrically evoked responses of the human cortex before and after cochlear implantation
Hearing Research 171 (2002) 191^195 www.elsevier.com/locate/heares
Acoustically and electrically evoked responses of the human cortex before and after cochlear implantation C. Pantev
d;
, B. Ross
a;d
, A. Wollbrink a;d , M. Riebandt b , K.W. Delank c , E. Seifert e , A. Lamprecht-Dinnesen b
a
Institute of Experimental Audiology, Mu«nster University Hospital, Mu«nster, Germany Department of Phoniatrics and Pediatric Audiology, Mu«nster University Hospital, Mu«nster, Germany c ENT Department, Mu«nster University Hospital, Mu«nster, Germany Rotman Research Institute for Neuroscience, Baycrest Centre for Geriatric Care, Canada Research Chair ‘Human Cortical Plasticity’, University of Toronto, 3560 Bathurst Street, Toronto, ON, Canada M6A 2E1 e Division of Phoniatrics, ENT Department, University of Berne, Berne, Switzerland b
d
Received 22 January 2002; accepted 24 May 2002
Abstract Multi-channel auditory evoked potentials (AEP) were recorded before and after cochlear implantation (CI) from a patient suffering from severe high frequency hearing loss with residual, but highly fluctuating hearing around 250 Hz. Immediately after CI activation early components of the N1 were present. Later N1 components developed during the use of CI. The unique result of this single case study is the concordance of the cortical AEP pattern obtained by native and artificial peripheral stimulation, which can be regarded as an indicator for the adequate function of the CI. 6 2002 Elsevier Science B.V. All rights reserved. Key words: Auditory evoked potential; Cochlear implant; Human auditory cortex; Cortical plasticity
1. Introduction The cochlear implant (CI) has been clinically available since 1984, restoring hearing in subjects with profound hearing loss. Multi-channel intra-cochlear electrode arrays have been developed in order to provide pitch perception and speech recognition. The signalprocessing strategies implemented in current CI systems are intended to stimulate the auditory nerve in such a manner that spectral and temporal information of the acoustic signal is represented adequately. The majority of CI users obtain satisfying clinical results. However, performance varies widely, ranging from simple detec-
tion of sounds to full understanding of speech (Tyler et al., 1995). Up to now, there has been no unique factor known for predicting the post-operative performance, but biographical data such as duration of deafness and age at implantation may be very important factors (Van Dijk et al., 1999). The aim of this study was to compare in a unique case the evoked potentials of the auditory cortex elicited by a still functional part of the cochlea, and by a CI in the same patient. The similarity of the cortical activation evoked by the native and the arti¢cial stimulation was expected to serve as an estimate of the adequacy of the CI.
2. Methods * Corresponding author. Tel.: +1 (416) 785 2500 ext. 2690; Fax: +1 (416) 785 2862. E-mail address: [email protected] (C. Pantev).
2.1. Subject
Abbreviations: AEP, auditory evoked potential; CI, cochlear implant; N1, major component of the AEP with a latency of about 100 ms after the stimulus onset; FMW test, Freiburg monosyllabic word test; EOG, electrooculogram
This study was carried out in a 55 year old male, who showed pre-operatively an extremely £uctuating and progressively profound hearing loss, and an intensive
0378-5955 / 02 / $ ^ see front matter 6 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 5 9 5 5 ( 0 2 ) 0 0 5 1 1 - 7
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C. Pantev et al. / Hearing Research 171 (2002) 191^195
tinnitus of unknown etiology. The duration of severeto-profound hearing loss in both ears was longer than 30 years. Five years prior to the implantation the subject had a sudden hearing loss. Pre-operatively the pure tone threshold of the better (right) ear demonstrated a sharp decay from 30 dB normative hearing level (nHL) at 250 Hz to 100 dB nHL at 1.5 kHz. The aided speech perception ability ranged from zero to 15% in the Freiburg monosyllabic word (FMW) test. The subject’s voice and speech-related results were normal. A Nucleus CI 24M cochlear implant was inserted in his right ear. The input dynamic range of the speech processor covers 35 dB, implementing an automatic gain control in the high level region. In the normal con¢guration all 22 mono-polar electrodes were activated with 14 400 pulses per second. 2.2. Stimulation In multiple measurement trials we succeeded once in recording auditory evoked potentials (AEP) 2 months before implantation. Three subsequent measurements were carried out after implantation (Miyamoto, 1986; Brix and Gedlicka, 1991; Ponton et al., 1993). The ¢rst post-implantation measurement was made on the day of initial CI processor setup. The following measurements were made 55 and 95 days thereafter. The stimuli were 250 Hz tone-bursts with a cosine-shaped rise and decay of 10 ms duration and a 480 ms plateau. These stimuli were presented with a randomized inter-stimulus interval between 2.5 and 3.5 s. For the pre-implantation measurement the stimulus intensity was set at 90 dB nHL, which for a limited time was 60 dB above the subjective 250 Hz hearing threshold. Due to the restricted dynamic range of the CI device, the intensity could not be set in the same way for the post-implantation as for the pre-implantation measurement. The stimulus intensity was adjusted instead, according to the subjective loudness between four (loud) and ¢ve (very loud) on a scale ranging from one to six. During the pre-implantation measurement the stimuli were presented by a compressor driver speaker (Renkus Heinz Inc.), connected through a plastic tube and a silicon earpiece to the subject’s right ear. The acoustic delay was carefully compensated by an appropriate shift of the trigger signal. For the post-implantation measurements the electrical stimulus signal was passed through an isolation transformer to the CI processor input. In this mode the CI microphone was turned o¡ and thus artefacts from environmental noise were inhibited. The total number of acoustic stimuli in the pre-implantation session was 128, whereas 600 stimuli were applied in the post-implantation sessions. The pure tone stimulus was chosen instead of more complex stimuli such as speech for two main reasons.
Firstly, a speech signal that passes the normal auditory periphery may be quite di¡erent from a speech signal that is transformed and transmitted by a CI, especially in this case of extremely unstable pure tone threshold. Secondly, it is more di⁄cult to separate the stimulus artifact produced by a complex speech signal from the AEP peaks of interest than for a simpler tonal signal. The reason for choosing a relatively low frequency stimulus of 250 Hz was that the residual hearing of the patient was in this frequency range. Even though the residual hearing was highly £uctuating, reliable AEP has been recorded. The implant electrodes activated by the 250 Hz tonal stimuli were the most apical ones. Though the electrode array was inserted completely into the cochlea, the most apical electrode may reach a place originally designated to frequencies not much below 1000 Hz. However, the CI restores low frequency pitch perception completely (Chen et al., 1999; Rauschecker and Shannon, 2002). Therefore, the 250 Hz tone was an appropriate stimulus in the post-implantation measurement even when di¡erent ¢bers of the hearing nerve were stimulated electrically as well as acoustically before implantation. 2.3. Data acquisition All measurements were carried out in an acoustically and electrically shielded room. The patient was watching a self-selected video cartoon in order to keep him alert during the measurement session. The electroencephalogram was recorded with a 32 Ag/AgCl electrode cap connected to a 32 channel ampli¢er (Neuroscan). The electrode placement was based on the 19 electrodes of the international 10-20 system, and 11 electrodes were added at temporal, frontal and mastoid sites. The impedances of all electrodes were below 5 k6 at 10 Hz. The reference electrode was placed on the nose, and the ground electrode on the forehead. Vertical eye movements were monitored by two bipolar electrooculogram (EOG) electrodes, placed above and below the eye, whereas horizontal eye movements were recorded by electrodes placed on the outer canthus of each eye. 2.4. Data-processing In the pre-implantation session, trials containing an EOG artifact were rejected on an individual channel basis using a 200 WV peak-to-peak threshold criterion. In the post-implantation sessions the threshold was increased to 400 WV for some ipsilateral channels, because of the large stimulus artefact produced by the CI. The artifact-free trials in the pre-operative and post-operative sessions were averaged over a 500 ms period, including a 100 ms pre-stimulus interval. After removal of the DC o¡set, which was estimated from the pre-stim-
HEARES 3956 15-8-02
C. Pantev et al. / Hearing Research 171 (2002) 191^195
ulus interval, the averaged data were 30 Hz low-pass ¢ltered. In the post-implantation measurements the data obtained from the left hemisphere (contralateral to the CI) contained no stimulus artefacts. Therefore, these data were treated in the same way as the data from the pre-implantation measurement. In order to reduce the stimulus artifact, further processing steps including muting during stimulus transition, o¡set correction and trend removal were applied to the right hemisphere data from the post-implantation measurements. The data of all recording sessions were visualized with respect to an averaged reference. The timeseries of the RMS-values across all left hemisphere channels, including those on the central line, was calculated after removal of the mean in order to allow a quantitative comparison of the evoked activity between consecutive measurements.
3. Results Immediately after activating the CI device the patient scored 40% correct in the FMW test, and his score increased to 90% 3 months later. Speech and hearing therapy focused on speech perception in noise, espe-
193
cially on the di¡erentiation of minimal pairs. During the ¢rst 6 months with the CI, the patient’s loudness perception £uctuated similarly to his pre-operative status. Nevertheless, his pure tone audiogram was stable and ranged from 40 O 5 dB in the low frequency region to 30 O 5 dB above 1 kHz. The tinnitus disappeared almost completely. The subject is now able to use the telephone and to communicate exclusively in auditoryverbal manner, even at conferences and in noisy environments. In this unique study, it was possible to record the cortical AEP from the same individual before and after CI. As expected, the data from the right hemisphere, ipsilateral to the CI, were strongly contaminated by artifacts, which was not the case for the data from the contralateral left hemisphere. The N1 component of the AEP with latencies around 100 ms was clearly identi¢ed in all recordings before and after implantation. The time series of AEP before and 3 months after implantation are shown in Fig. 1c in the electrode con¢guration layout. The distribution of the N1 response showed two dipolar formations with positive maxima at the posterior temporal channels and overlapping negative minima in the central frontal channels. The distri-
Fig. 1. AEP time series obtained before and after implantation. (a) Di¡erence between channels M1 and Cz before implantation, at the day of initial setup and 95 days thereafter. (b) RMS values across all channels of left hemisphere and central line. The vertical lines in panels a and b mark latencies of 90 and 120 ms, respectively. (c) 31 channel time series of native AEP, and AEP after 95 days of CI usage. The label ‘CI’ denotes schematically the position of the CI device in the right hemisphere.
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butions were similar for the pre- and post-implantation AEP with a tendency for more frontal shift of the negative N1 maximum after CI use. The native N1 response showed a double peak con¢guration with peak latencies of 90 and 120 ms. The 120 ms component of the N1 response was of larger amplitude compared to the earlier component especially in the central channels of maximum negativity. Only at the posterior electrodes were the 90 and 120 ms components of about the same amplitude. The AEP elicited by the CI stimulation showed remarkably similar N1 double peak con¢guration with the same peak latencies as obtained in the preimplantation measurement. In general the amplitudes of the N1 response after implantation were somewhat smaller at the central electrodes, whereas they were larger at the temporal electrodes. The time series of the di¡erences between Cz and M1 electrodes (maximally responding channels of opposite polarity in the left hemisphere, contralateral to stimulation) are shown in Fig. 1a. The AEP obtained immediately after initial CI activation reached its amplitude maximum with a latency of 90 ms. The peak amplitude resembled that of the pre-implantation response at this latency. In contrast, at a latency of 120 ms, the peak of the ¢rst day response was about half the amplitude of the pre-implantation response. Almost no di¡erences were observed between the responses obtained after 55 and 95 days of CI use. Therefore, the 55 day responses were omitted for clarity from Fig. 1a. After 95 days of using the CI, the 90 ms component showed similar amplitude compared to the previous measurements. In contrast the 120 ms component was still smaller as compared to the pre-implantation measurement. A quantitative comparison of the N1 activity before and after implantation, based on single channel data as shown in Fig. 1a, may not be representative of the changes of the AEP distribution between measurements. Therefore, the RMS values across the left hemisphere channels have been calculated. The result is a measure of the mean signal power of all included channels regardless of the ¢eld distribution. The time course of the RMS values is shown in Fig. 1b for all measurements. The speci¢c double-peaked N1 response before implantation can also be observed here. At a latency of 90 ms, the responses elicited by the CI reproduced the amplitude of the response before implantation to a high degree. At 120 ms the initial CI response reached only 50% of the response power before implantation. After 55 days of CI use the amplitude of the 120 ms component increased, but still did not reach the amplitude obtained before implantation. The waveforms obtained 55 and 95 days after CI initialization do not demonstrate further change in signal power. Another observation is the increase of the signal power around 200 ms (corresponding to the P2 response) with continuous use
of the CI device that exceeds the values obtained before implantation.
4. Discussion Di¡erent parameters of the electric stimulus, including frequency content, stimulation rate and pulse shape e¡ect the stimulation of the auditory nerve via the CI. In this subject, the peak latencies of the AEP waveforms, the amplitude of the early N1 component and their topography across the scalp were consistent and similar between native acoustic stimulation and electric stimulation using the CI. These facts may be interpreted as evidence that the chosen CI stimulation parameters were adequate for eliciting a cortical representation similar to normal hearing. Immediately after the initial CI activation, the 90 ms component of the N1 response reached the same value that was observed during the pre-implantation measurement. Measurements after 55 and 95 days of CI use also replicated the 90 ms amplitude almost exactly. In contrast, variations of the N1 activity were observed in the latency range between 90 and 120 ms. It is well accepted that the N1 response consists of di¡erent components with di¡erent functional meaning (Na«a«ta«nen and Picton, 1987). The early components of the N1 are more likely related to physical parameters of the auditory stimulus and re£ect more directly the sensory input, whereas the later components of the N1 are of more endogenous nature. The observed behavior of the early N1 component demonstrated that cortical areas were activated immediately after the connection to the sensory input had been restored. Jordan et al. (1997) showed that the latency of N1 response to 1450 Hz pure tone bursts decreased to normal values during the ¢rst month of CI use in postlingually deaf patients. The latencies of the absolute N1 peaks in this study lead to a contradictory ¢nding. The N1 latency increased with the time of CI use towards the N1 latency obtained from the pre-implantation measurement. However, the double peak con¢guration of the N1 response is an indicator of multiple components. These components seem to develop di¡erently over the time of CI use. The results shown here demonstrate that the global N1 peak amplitude and latency have to be discussed very carefully. Nevertheless, consistent with the results of Jordan et al. (1997), the cortical responses seem to develop towards a normal con¢guration. The global power of the N1 activity increased between measurements that were carried out immediately after CI initialization and after 55 days of CI use. The AEP obtained after 95 days reproduced the measurement carried out after 55 days almost exactly. How-
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ever, the N1 activity remained smaller compared to the pre-implantation observation. Therefore, the question should be asked whether further improvement of CI adjustment and the patient’s post-implantation training could help to reach the cortical activation observed before implantation. The patient su¡ered from a profound high frequency hearing loss. Consequently, wide areas of the auditory cortex were deprived of their sensory inputs. It can be assumed that cortical reorganization resulted in a wider representation of the low frequencies due to the invasion of their sensory inputs towards cortical areas designated previously to higher frequency inputs. After implantation pitch perception was restored correspondingly to almost the entire frequency range of normal hearing. Even low frequencies, for which corresponding hearing nerve ¢bers were not directly stimulated, obtain their cortical representation from combination of higher harmonics (Rauschecker and Shannon, 2002). Extended cortical areas are no longer available for exclusive processing of low frequency sounds. It is likely that the highly reproducible N1 responses at 55 and 95 days after CI activation already demonstrate the optimal cortical representation of the 250 Hz input. The results of this single case study provide evidence that in cases where cortical AEP can be recorded before implantation, even in response to a very limited stimulus frequency range, similar responses from the auditory cortex can be obtained after implantation. This can be regarded as an indicator of the adequate function of the CI. However, the patient’s bene¢ts were much better than just restoring hearing at low frequencies because the CI provided him with access to the entire frequency range useful for communication. In the rare cases in which it is possible to perform successful AEP recording during pre-implantation diagnostics, such recordings can provide valuable evidence for successful recovery of hearing performance during the use of the
195
CI. The post-implantation measurements illustrated the development of the evoked cortical responses. The high degree of consistency with the native N1 response demonstrated the adequateness of the CI stimulation. Even if pre-implantation AEP are not feasible, AEP recordings may be helpful during the CI adjustment process. Also the application of multi-channel recording seems reasonable since it allows the observation of structural details of the AEP that are not available during single channel recording. References Brix, R., Gedlicka, W., 1991. Late cortical auditory potentials evoked by electrostimulation in deaf and cochlear implant patients. Eur. Arch. Otorhinolaryngol. 248, 442^444. Chen, J.M., Farb, R., Hanusaik, L., Shipp, D., Nedzelski, J.M., 1999. Depth and quality of electrode insertion: a radiologic and pitch scaling assessment of two cochlear implant systems. Am. J. Otol. 20, 192^197. Jordan, K., Schmidt, A., Plotz, K., von Specht, H., Begall, K., Roth, N., Scheich, H., 1997. Auditory event-related potentials in postand prelingually deaf cochlear implant recipients. Am. J. Otol. 18, S116^S117. Miyamoto, R.T., 1986. Electrically evoked potentials in cochlear implant subjects. Laryngoscope 96, 178^185. Na«a«ta«nen, R., Picton, T.W., 1987. The N1 wave of the human electric and magnetic response to sound: A review and an analysis of the component structure. Psychophysiology 24, 375^425. Ponton, C., Don, M., Waring, M., Eggermont, J., Masuda, A., 1993. Spatio-temporal source modeling of evoked potentials to acoustic and cochlear implant stimulation. Electroencephalogr. Clin. Neurophysiol. 88, 478^493. Rauschecker, J.P., Shannon, R.V., 2002. Sending sound to the brain. Science 295, 1025^1029. Tyler, R.S., Lowder, M.W., Parkinson, A.J., Woodworth, G.G., Gantz, B.J., 1995. Performance of adult Ineraid and Nucleus cochlear implant patients after 3.5 years of use. Audiology 34, 135^ 144. Van Dijk, J.E., van Olphen, A.F., Langereis, M.C., Mens, L.H., Brokx, J.P., Smoorenburg, G.F., 1999. Predictors of cochlear implant performance. Audiology 38, 109^116.
HEARES 3956 15-8-02
Acoustically and electrically evoked responses of the human cortex before and after cochlear implantation C. Pantev
d;
, B. Ross
a;d
, A. Wollbrink a;d , M. Riebandt b , K.W. Delank c , E. Seifert e , A. Lamprecht-Dinnesen b
a
Institute of Experimental Audiology, Mu«nster University Hospital, Mu«nster, Germany Department of Phoniatrics and Pediatric Audiology, Mu«nster University Hospital, Mu«nster, Germany c ENT Department, Mu«nster University Hospital, Mu«nster, Germany Rotman Research Institute for Neuroscience, Baycrest Centre for Geriatric Care, Canada Research Chair ‘Human Cortical Plasticity’, University of Toronto, 3560 Bathurst Street, Toronto, ON, Canada M6A 2E1 e Division of Phoniatrics, ENT Department, University of Berne, Berne, Switzerland b
d
Received 22 January 2002; accepted 24 May 2002
Abstract Multi-channel auditory evoked potentials (AEP) were recorded before and after cochlear implantation (CI) from a patient suffering from severe high frequency hearing loss with residual, but highly fluctuating hearing around 250 Hz. Immediately after CI activation early components of the N1 were present. Later N1 components developed during the use of CI. The unique result of this single case study is the concordance of the cortical AEP pattern obtained by native and artificial peripheral stimulation, which can be regarded as an indicator for the adequate function of the CI. 6 2002 Elsevier Science B.V. All rights reserved. Key words: Auditory evoked potential; Cochlear implant; Human auditory cortex; Cortical plasticity
1. Introduction The cochlear implant (CI) has been clinically available since 1984, restoring hearing in subjects with profound hearing loss. Multi-channel intra-cochlear electrode arrays have been developed in order to provide pitch perception and speech recognition. The signalprocessing strategies implemented in current CI systems are intended to stimulate the auditory nerve in such a manner that spectral and temporal information of the acoustic signal is represented adequately. The majority of CI users obtain satisfying clinical results. However, performance varies widely, ranging from simple detec-
tion of sounds to full understanding of speech (Tyler et al., 1995). Up to now, there has been no unique factor known for predicting the post-operative performance, but biographical data such as duration of deafness and age at implantation may be very important factors (Van Dijk et al., 1999). The aim of this study was to compare in a unique case the evoked potentials of the auditory cortex elicited by a still functional part of the cochlea, and by a CI in the same patient. The similarity of the cortical activation evoked by the native and the arti¢cial stimulation was expected to serve as an estimate of the adequacy of the CI.
2. Methods * Corresponding author. Tel.: +1 (416) 785 2500 ext. 2690; Fax: +1 (416) 785 2862. E-mail address: [email protected] (C. Pantev).
2.1. Subject
Abbreviations: AEP, auditory evoked potential; CI, cochlear implant; N1, major component of the AEP with a latency of about 100 ms after the stimulus onset; FMW test, Freiburg monosyllabic word test; EOG, electrooculogram
This study was carried out in a 55 year old male, who showed pre-operatively an extremely £uctuating and progressively profound hearing loss, and an intensive
0378-5955 / 02 / $ ^ see front matter 6 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 5 9 5 5 ( 0 2 ) 0 0 5 1 1 - 7
HEARES 3956 15-8-02
192
C. Pantev et al. / Hearing Research 171 (2002) 191^195
tinnitus of unknown etiology. The duration of severeto-profound hearing loss in both ears was longer than 30 years. Five years prior to the implantation the subject had a sudden hearing loss. Pre-operatively the pure tone threshold of the better (right) ear demonstrated a sharp decay from 30 dB normative hearing level (nHL) at 250 Hz to 100 dB nHL at 1.5 kHz. The aided speech perception ability ranged from zero to 15% in the Freiburg monosyllabic word (FMW) test. The subject’s voice and speech-related results were normal. A Nucleus CI 24M cochlear implant was inserted in his right ear. The input dynamic range of the speech processor covers 35 dB, implementing an automatic gain control in the high level region. In the normal con¢guration all 22 mono-polar electrodes were activated with 14 400 pulses per second. 2.2. Stimulation In multiple measurement trials we succeeded once in recording auditory evoked potentials (AEP) 2 months before implantation. Three subsequent measurements were carried out after implantation (Miyamoto, 1986; Brix and Gedlicka, 1991; Ponton et al., 1993). The ¢rst post-implantation measurement was made on the day of initial CI processor setup. The following measurements were made 55 and 95 days thereafter. The stimuli were 250 Hz tone-bursts with a cosine-shaped rise and decay of 10 ms duration and a 480 ms plateau. These stimuli were presented with a randomized inter-stimulus interval between 2.5 and 3.5 s. For the pre-implantation measurement the stimulus intensity was set at 90 dB nHL, which for a limited time was 60 dB above the subjective 250 Hz hearing threshold. Due to the restricted dynamic range of the CI device, the intensity could not be set in the same way for the post-implantation as for the pre-implantation measurement. The stimulus intensity was adjusted instead, according to the subjective loudness between four (loud) and ¢ve (very loud) on a scale ranging from one to six. During the pre-implantation measurement the stimuli were presented by a compressor driver speaker (Renkus Heinz Inc.), connected through a plastic tube and a silicon earpiece to the subject’s right ear. The acoustic delay was carefully compensated by an appropriate shift of the trigger signal. For the post-implantation measurements the electrical stimulus signal was passed through an isolation transformer to the CI processor input. In this mode the CI microphone was turned o¡ and thus artefacts from environmental noise were inhibited. The total number of acoustic stimuli in the pre-implantation session was 128, whereas 600 stimuli were applied in the post-implantation sessions. The pure tone stimulus was chosen instead of more complex stimuli such as speech for two main reasons.
Firstly, a speech signal that passes the normal auditory periphery may be quite di¡erent from a speech signal that is transformed and transmitted by a CI, especially in this case of extremely unstable pure tone threshold. Secondly, it is more di⁄cult to separate the stimulus artifact produced by a complex speech signal from the AEP peaks of interest than for a simpler tonal signal. The reason for choosing a relatively low frequency stimulus of 250 Hz was that the residual hearing of the patient was in this frequency range. Even though the residual hearing was highly £uctuating, reliable AEP has been recorded. The implant electrodes activated by the 250 Hz tonal stimuli were the most apical ones. Though the electrode array was inserted completely into the cochlea, the most apical electrode may reach a place originally designated to frequencies not much below 1000 Hz. However, the CI restores low frequency pitch perception completely (Chen et al., 1999; Rauschecker and Shannon, 2002). Therefore, the 250 Hz tone was an appropriate stimulus in the post-implantation measurement even when di¡erent ¢bers of the hearing nerve were stimulated electrically as well as acoustically before implantation. 2.3. Data acquisition All measurements were carried out in an acoustically and electrically shielded room. The patient was watching a self-selected video cartoon in order to keep him alert during the measurement session. The electroencephalogram was recorded with a 32 Ag/AgCl electrode cap connected to a 32 channel ampli¢er (Neuroscan). The electrode placement was based on the 19 electrodes of the international 10-20 system, and 11 electrodes were added at temporal, frontal and mastoid sites. The impedances of all electrodes were below 5 k6 at 10 Hz. The reference electrode was placed on the nose, and the ground electrode on the forehead. Vertical eye movements were monitored by two bipolar electrooculogram (EOG) electrodes, placed above and below the eye, whereas horizontal eye movements were recorded by electrodes placed on the outer canthus of each eye. 2.4. Data-processing In the pre-implantation session, trials containing an EOG artifact were rejected on an individual channel basis using a 200 WV peak-to-peak threshold criterion. In the post-implantation sessions the threshold was increased to 400 WV for some ipsilateral channels, because of the large stimulus artefact produced by the CI. The artifact-free trials in the pre-operative and post-operative sessions were averaged over a 500 ms period, including a 100 ms pre-stimulus interval. After removal of the DC o¡set, which was estimated from the pre-stim-
HEARES 3956 15-8-02
C. Pantev et al. / Hearing Research 171 (2002) 191^195
ulus interval, the averaged data were 30 Hz low-pass ¢ltered. In the post-implantation measurements the data obtained from the left hemisphere (contralateral to the CI) contained no stimulus artefacts. Therefore, these data were treated in the same way as the data from the pre-implantation measurement. In order to reduce the stimulus artifact, further processing steps including muting during stimulus transition, o¡set correction and trend removal were applied to the right hemisphere data from the post-implantation measurements. The data of all recording sessions were visualized with respect to an averaged reference. The timeseries of the RMS-values across all left hemisphere channels, including those on the central line, was calculated after removal of the mean in order to allow a quantitative comparison of the evoked activity between consecutive measurements.
3. Results Immediately after activating the CI device the patient scored 40% correct in the FMW test, and his score increased to 90% 3 months later. Speech and hearing therapy focused on speech perception in noise, espe-
193
cially on the di¡erentiation of minimal pairs. During the ¢rst 6 months with the CI, the patient’s loudness perception £uctuated similarly to his pre-operative status. Nevertheless, his pure tone audiogram was stable and ranged from 40 O 5 dB in the low frequency region to 30 O 5 dB above 1 kHz. The tinnitus disappeared almost completely. The subject is now able to use the telephone and to communicate exclusively in auditoryverbal manner, even at conferences and in noisy environments. In this unique study, it was possible to record the cortical AEP from the same individual before and after CI. As expected, the data from the right hemisphere, ipsilateral to the CI, were strongly contaminated by artifacts, which was not the case for the data from the contralateral left hemisphere. The N1 component of the AEP with latencies around 100 ms was clearly identi¢ed in all recordings before and after implantation. The time series of AEP before and 3 months after implantation are shown in Fig. 1c in the electrode con¢guration layout. The distribution of the N1 response showed two dipolar formations with positive maxima at the posterior temporal channels and overlapping negative minima in the central frontal channels. The distri-
Fig. 1. AEP time series obtained before and after implantation. (a) Di¡erence between channels M1 and Cz before implantation, at the day of initial setup and 95 days thereafter. (b) RMS values across all channels of left hemisphere and central line. The vertical lines in panels a and b mark latencies of 90 and 120 ms, respectively. (c) 31 channel time series of native AEP, and AEP after 95 days of CI usage. The label ‘CI’ denotes schematically the position of the CI device in the right hemisphere.
HEARES 3956 15-8-02
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C. Pantev et al. / Hearing Research 171 (2002) 191^195
butions were similar for the pre- and post-implantation AEP with a tendency for more frontal shift of the negative N1 maximum after CI use. The native N1 response showed a double peak con¢guration with peak latencies of 90 and 120 ms. The 120 ms component of the N1 response was of larger amplitude compared to the earlier component especially in the central channels of maximum negativity. Only at the posterior electrodes were the 90 and 120 ms components of about the same amplitude. The AEP elicited by the CI stimulation showed remarkably similar N1 double peak con¢guration with the same peak latencies as obtained in the preimplantation measurement. In general the amplitudes of the N1 response after implantation were somewhat smaller at the central electrodes, whereas they were larger at the temporal electrodes. The time series of the di¡erences between Cz and M1 electrodes (maximally responding channels of opposite polarity in the left hemisphere, contralateral to stimulation) are shown in Fig. 1a. The AEP obtained immediately after initial CI activation reached its amplitude maximum with a latency of 90 ms. The peak amplitude resembled that of the pre-implantation response at this latency. In contrast, at a latency of 120 ms, the peak of the ¢rst day response was about half the amplitude of the pre-implantation response. Almost no di¡erences were observed between the responses obtained after 55 and 95 days of CI use. Therefore, the 55 day responses were omitted for clarity from Fig. 1a. After 95 days of using the CI, the 90 ms component showed similar amplitude compared to the previous measurements. In contrast the 120 ms component was still smaller as compared to the pre-implantation measurement. A quantitative comparison of the N1 activity before and after implantation, based on single channel data as shown in Fig. 1a, may not be representative of the changes of the AEP distribution between measurements. Therefore, the RMS values across the left hemisphere channels have been calculated. The result is a measure of the mean signal power of all included channels regardless of the ¢eld distribution. The time course of the RMS values is shown in Fig. 1b for all measurements. The speci¢c double-peaked N1 response before implantation can also be observed here. At a latency of 90 ms, the responses elicited by the CI reproduced the amplitude of the response before implantation to a high degree. At 120 ms the initial CI response reached only 50% of the response power before implantation. After 55 days of CI use the amplitude of the 120 ms component increased, but still did not reach the amplitude obtained before implantation. The waveforms obtained 55 and 95 days after CI initialization do not demonstrate further change in signal power. Another observation is the increase of the signal power around 200 ms (corresponding to the P2 response) with continuous use
of the CI device that exceeds the values obtained before implantation.
4. Discussion Di¡erent parameters of the electric stimulus, including frequency content, stimulation rate and pulse shape e¡ect the stimulation of the auditory nerve via the CI. In this subject, the peak latencies of the AEP waveforms, the amplitude of the early N1 component and their topography across the scalp were consistent and similar between native acoustic stimulation and electric stimulation using the CI. These facts may be interpreted as evidence that the chosen CI stimulation parameters were adequate for eliciting a cortical representation similar to normal hearing. Immediately after the initial CI activation, the 90 ms component of the N1 response reached the same value that was observed during the pre-implantation measurement. Measurements after 55 and 95 days of CI use also replicated the 90 ms amplitude almost exactly. In contrast, variations of the N1 activity were observed in the latency range between 90 and 120 ms. It is well accepted that the N1 response consists of di¡erent components with di¡erent functional meaning (Na«a«ta«nen and Picton, 1987). The early components of the N1 are more likely related to physical parameters of the auditory stimulus and re£ect more directly the sensory input, whereas the later components of the N1 are of more endogenous nature. The observed behavior of the early N1 component demonstrated that cortical areas were activated immediately after the connection to the sensory input had been restored. Jordan et al. (1997) showed that the latency of N1 response to 1450 Hz pure tone bursts decreased to normal values during the ¢rst month of CI use in postlingually deaf patients. The latencies of the absolute N1 peaks in this study lead to a contradictory ¢nding. The N1 latency increased with the time of CI use towards the N1 latency obtained from the pre-implantation measurement. However, the double peak con¢guration of the N1 response is an indicator of multiple components. These components seem to develop di¡erently over the time of CI use. The results shown here demonstrate that the global N1 peak amplitude and latency have to be discussed very carefully. Nevertheless, consistent with the results of Jordan et al. (1997), the cortical responses seem to develop towards a normal con¢guration. The global power of the N1 activity increased between measurements that were carried out immediately after CI initialization and after 55 days of CI use. The AEP obtained after 95 days reproduced the measurement carried out after 55 days almost exactly. How-
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ever, the N1 activity remained smaller compared to the pre-implantation observation. Therefore, the question should be asked whether further improvement of CI adjustment and the patient’s post-implantation training could help to reach the cortical activation observed before implantation. The patient su¡ered from a profound high frequency hearing loss. Consequently, wide areas of the auditory cortex were deprived of their sensory inputs. It can be assumed that cortical reorganization resulted in a wider representation of the low frequencies due to the invasion of their sensory inputs towards cortical areas designated previously to higher frequency inputs. After implantation pitch perception was restored correspondingly to almost the entire frequency range of normal hearing. Even low frequencies, for which corresponding hearing nerve ¢bers were not directly stimulated, obtain their cortical representation from combination of higher harmonics (Rauschecker and Shannon, 2002). Extended cortical areas are no longer available for exclusive processing of low frequency sounds. It is likely that the highly reproducible N1 responses at 55 and 95 days after CI activation already demonstrate the optimal cortical representation of the 250 Hz input. The results of this single case study provide evidence that in cases where cortical AEP can be recorded before implantation, even in response to a very limited stimulus frequency range, similar responses from the auditory cortex can be obtained after implantation. This can be regarded as an indicator of the adequate function of the CI. However, the patient’s bene¢ts were much better than just restoring hearing at low frequencies because the CI provided him with access to the entire frequency range useful for communication. In the rare cases in which it is possible to perform successful AEP recording during pre-implantation diagnostics, such recordings can provide valuable evidence for successful recovery of hearing performance during the use of the
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CI. The post-implantation measurements illustrated the development of the evoked cortical responses. The high degree of consistency with the native N1 response demonstrated the adequateness of the CI stimulation. Even if pre-implantation AEP are not feasible, AEP recordings may be helpful during the CI adjustment process. Also the application of multi-channel recording seems reasonable since it allows the observation of structural details of the AEP that are not available during single channel recording. References Brix, R., Gedlicka, W., 1991. Late cortical auditory potentials evoked by electrostimulation in deaf and cochlear implant patients. Eur. Arch. Otorhinolaryngol. 248, 442^444. Chen, J.M., Farb, R., Hanusaik, L., Shipp, D., Nedzelski, J.M., 1999. Depth and quality of electrode insertion: a radiologic and pitch scaling assessment of two cochlear implant systems. Am. J. Otol. 20, 192^197. Jordan, K., Schmidt, A., Plotz, K., von Specht, H., Begall, K., Roth, N., Scheich, H., 1997. Auditory event-related potentials in postand prelingually deaf cochlear implant recipients. Am. J. Otol. 18, S116^S117. Miyamoto, R.T., 1986. Electrically evoked potentials in cochlear implant subjects. Laryngoscope 96, 178^185. Na«a«ta«nen, R., Picton, T.W., 1987. The N1 wave of the human electric and magnetic response to sound: A review and an analysis of the component structure. Psychophysiology 24, 375^425. Ponton, C., Don, M., Waring, M., Eggermont, J., Masuda, A., 1993. Spatio-temporal source modeling of evoked potentials to acoustic and cochlear implant stimulation. Electroencephalogr. Clin. Neurophysiol. 88, 478^493. Rauschecker, J.P., Shannon, R.V., 2002. Sending sound to the brain. Science 295, 1025^1029. Tyler, R.S., Lowder, M.W., Parkinson, A.J., Woodworth, G.G., Gantz, B.J., 1995. Performance of adult Ineraid and Nucleus cochlear implant patients after 3.5 years of use. Audiology 34, 135^ 144. Van Dijk, J.E., van Olphen, A.F., Langereis, M.C., Mens, L.H., Brokx, J.P., Smoorenburg, G.F., 1999. Predictors of cochlear implant performance. Audiology 38, 109^116.
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