To examine the maturational status of the auditory cortex in adults with cochlear implants (CIs) using the latencies of the P1, N1, and P2 components of cortical auditory-evoked potentials (CAEPs).
A total of 25 adults with CIs and 25 age-matched, normal-hearing control subjects participated in this study. Specifically, patients with CIs were divided into three groups depending on their age of deafness onset: Group A comprised patients with prelingual deafness who had received CI during early childhood (n=7), Group B comprised patients with early childhood-onset, progressive deafness who had received CI during childhood (n=6), and Group C comprised patients with adult-onset deafness (n=12). The P1, N1, and P2 latencies of their CAEPs were then compared between CI patients and normal-hearing subjects.
All participants showed clear CAEP responses. P1 and N1 latencies in Group A and Group C patients were significantly longer than those in the control group. Meanwhile, Group B patients had significantly longer N1 and P2 latencies, as compared with those in the control group.
Patients with prelingual deafness and those with early-childhood onset, progressive deafness who received CI developed primary and higher-order auditory areas postoperatively when they became adults. However, their auditory cortex maturational statuses seemed to be worse than that of normal-hearing individuals. Furthermore, adult patients with late-onset deafness might experience degenerative auditory cortex changes during the auditory deprivation period between deafness onset and cochlear implantation.
The brain is underdeveloped at birth and cortical development is dependent on extrinsic stimulation. Sufficient auditory input should be provided for appropriate development of the auditory cortex during the sensitive period when neuroplasticity of the auditory cortex is at a maximum [
Cortical auditory evoked potentials (CAEPs) can be used to assess the maturational status of the auditory cortex [
A cochlear implant (CI) effectively restores the auditory function of patients with cochlear hearing loss. There have been several studies showing the maturation of CAEPs following CI surgery in deaf children [
Fifty subjects including 25 patients with CIs and 25 subjects with normal hearing participated in this study. All the participants were adults (age 18 years or older) except two patients with CI whose ages were 17 years old.
The mean age of 25 patients with CIs was 38.4 years (range 17-79 years). They were divided into three groups depending on the age of onset of deafness. Group A, patients with prelingual deafness who had received CI during early childhood (n=7); group B, patients with early childhood-onset, progressive deafness who received CI during childhood (n=6); and group C, patients with adult-onset deafness (n=12). The median deaf duration, the time interval between onset of deafness and CI surgery were 6.1 years in group A, 2.35 years in group B, and 6.75 years in group C. The median age at CI surgery were 6.1 years in group A, 16.55 years in group B, and 54.45 years in group C. The median age at participating in this study were 18 years in group A, 19 years in group B, 54.65 years in group C. All the patients had normal cochlea and normal cochlear nerve in imaging studies including temporal bone computed tomography and magnetic resonance images of the internal auditory canal. No one had brain parenchymal lesion in the imaging studies.
Twenty-five subjects with normal hearing for both ear were matched for age with the patients with CIs and served as controls. Normal hearing was defined as a pure-tone threshold better than or equal to 25 dB HL for octave frequencies between 250 Hz and 8,000 Hz. More details regarding demographics of the CI patients and the controls are provided in
None of the participants had a medical history of psychiatric, cognitive, or language-related diseases.
CAEPs were recorded from all participants. CI users wear their speech processors during the measurement. CAEPs were recorded in response to a 1,000 Hz tone burst sound. The duration of the sound stimulus was 100 ms (10 ms rise time, 80 ms plateau, and 10 ms fall time). Stimulation intensity was 80 dBnHL and stimulation rate was 0.7/s. We have found this intensity to be effective to elicit clear and robust CAEP [
The electroencephalographic response was collected using Viking IV (Nicolet Biomedical, Fenton, MO, USA). Scalp recordings were made using silver-coated surface-recording electrodes at midline (Fz; upper forehead) referenced to the contralateral mastoid. An electrode positioned at Fpz (lower forehead) was used as a ground. Eye blink was monitored using electrodes located above and below the eye contralateral to the test ear. Responses were amplified with a gain of 10,000 and filtered from 1 Hz (high-pass filter) to 30 Hz (low-pass filter). The recording window included a 50 ms prestimulus period and a 450 ms poststimulus period, and over 200 sweeps were obtained for each stimulus. Two CAEP waveforms for each stimulus were obtained to check reproducibility, and the mean latencies of each component of the CAEP were measured.
The latencies of P1, N1, and P2 components of the CAEP were compared between the patients with CIs and the participants with normal hearing. Analyses were performed using linear regression analysis, an independent t test, Kruskal-Wallis test, or Mann-Whitney U test using SPSS version 21.0 statistical software (IBM Corp., Armonk, NY, USA).
Typical CAEP waveforms recorded from a patient with a CI and a subject with normal hearing are presented in
The mean latencies of P1, N1, and P2 of patients with a CI and control subjects with normal hearing were presented in
P1 and N1 latencies of CI patients in group A were significantly longer than those of control participants with normal hearing (
The relationship between the latencies of each component of CAEPs and the duration of deafness in patients with a CI was assessed using linear regression analysis. No significant correlations were found between the latencies of P1, N1, and P2 and duration of deafness in all three groups (
Neuroplasticity of brain is an important factor determining the outcome of CI surgery for deaf patients. Because there is a sensitive period of increased neuroplasticity during which auditory cortex is maximally plastic, the final outcome of cochlear implantation is optimal when it is performed during this period sensitive for auditory cortical development: i.e., within the first 1-3 years of life [
P1 and N1 were recorded from every adult patient with prelingual deafness who received CI during early childhood and P2 was recorded in about two-thirds of them. These findings show that deaf children who received CI can develop their primary and higher-order auditory areas through electrical stimulation provided by the CI. However, their P1 and N1 latencies were significantly prolonged compared with those of control participants with normal hearing, which implies that maturation of the primary and higher-order auditory areas of patients with CI who participated in this study, is less optimal than it is in individuals with normal hearing. The one of the main reasons for the latency delay may be that the participants received CI when relatively older. Previous studies showed that there was a positive correlation between the age at CI and P1 latency in deaf children who received CI during early childhood [
The adult patients who had early childhood-onset, progressive deafness and who received CI during childhood showed clear P1, N1, and P2 responses. All of them had used hearing aids during early childhood because they had residual hearing at that time, and then received CI after losing their hearing progressively. Therefore, these patients may develop their auditory cortex with the aid of acoustic stimulation through hearing aids during early childhood and electrical stimulation through CI after losing their hearing. However, the maturational status of their auditory cortex seems worse than that of individuals with normal hearing as shown by their more prolonged N1 and P2 latencies.
Adults with late-onset deafness who received CI had significantly longer P1 and N1 latencies than control participants with normal hearing. This implies that the auditory cortex of adult patients with late-onset deafness undergoes degenerative change during any period of auditory deprivation. This finding is consistent with those of previous studies that have shown there is negative impact of the period of auditory deprivation on speech perception after cochlear implantation [
The purpose of this study was to reveal the CAEP findings of adults with CIs who had various past medical history concerned with hearing status. This study has some limitations. First one is that the number of participants is not enough. Second one is that this study is a cross sectional study. A longitudinal follow-up study including larger number of patients is better to examine the maturational status of auditory area of brain using CAEP. Third one is that patients with a CI included in this study were not homogenous in terms of age at CI surgery and CI use duration. Future study will recruit a larger number of adult patients with a CI and age-matched subjects with normal hearing and follow them up for a long period to come up with more solid conclusion.
In conclusion, patients with prelingual deafness and those with early-childhood onset, progressive deafness who received CI developed a primary and higher-order auditory areas when they reached adulthood, as shown by clear measurement of P1-N1-P2 of CAEPs. However, the latencies of each component of CAEP were more prolonged than those in individuals with normal hearing, which implies suboptimal development of a higher-order auditory areas. Adult-onset deafness was associated with prolonged P1 and N1 latencies after CI than in control participants with normal hearing, which possibly originates from auditory cortex degeneration because of auditory deprivation before CI surgery.
This study was supported by research funds from Dong-A University.
The authors have no financial conflicts of interest.
Conceptualization : Sung Wook Jeong. Data curation: Sung Wook Jeong, Seong-Hyun Boo. Formal analysis: Sung Wook Jeong, Seong-Hyun Boo. Methodology: Sung Wook Jeong. Project administration: Sung Wook Jeong. Visualization: Sung Wook Jeong. Writing—original draft: Seong-Hyun Boo. Writing—review & editing: Sung Wook Jeong, Seong-Hyun Boo. Approval of final manuscript: Sung Wook Jeong, Seong-Hyun Boo.
The representative CAEP waveforms obtained from a patient with a cochlear implant (CI) and an age-matched control participant with normal hearing. The latencies of P1, N1, and P2 of CI patient are longer than those of normal hearing subject. A: CAEP of a 25-year-old male patient who received a CI at the age of 10 years and 1 month. B: CAEP of a 25-year-old male participant with normal hearing.
Latencies of P1, N1, and P2 component of CAEP in patients with a cochlear implant (CI). There were no significant differences in the latencies between the three groups with a CI.
Comparison of latencies of P1, N1, and P2 between cochlear implant patients and control subjects. A: Latencies of P1, N1, and P2 of group A patients and control participants with normal hearing. The latencies of P1 and N1 of patients with a cochlear implant were significantly longer than those of control. B: Latencies of P1, N1, and P2 of group B patients and control participants with normal hearing. N1 and P2 latencies of patients with a cochlear implant were significantly longer than those of control. C: Latencies of P1, N1, and P2 of group C patients and control participants with normal hearing. The P1 and N1 latencies of patients with a cochlear implant were significantly longer than those in control subjects. *
Latencies of P1, N1, and P2 according to the duration of deafness in patients with a cochlear implant (CI). A: Prelingual deafness with CI. B: Early childhood-onset, progressive deafness with CI. C: Adult-onset deafness with CI. There was no significant correlation between the latencies and the duration of deafness.
Demographic data of patients with a CI and control participants with normal hearing
CI patients |
Control participants |
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No. | Etiology of HL | Age at HL onset (yr) | Age at deafness (yr) | Age at CI (yr) | Deaf duration (yr) | CI side | Preop. PTA (dB HL) | Age at CAEP test (yr) | CI use duration (yr) | No. | PTA (dB HL) | Age at CAEP test (yr) |
CI patients with prelingual deafness (Group A) | ||||||||||||
1 | Prematurity | 0 | 0 | 2.2 | 2.2 | Right | No data | 18 | 15.8 | 1 | 10 | 19 |
2 | Hereditary | 0 | 0 | 3.4 | 3.4 | Right | 92 | 17 | 13.6 | 2 | 10 | 19 |
3 | Unknown | 0 | 0 | 4.8 | 4.8 | Right | 92 | 18 | 13.2 | 3 | 10 | 18 |
4 | Unknown | 0 | 0 | 6.1 | 6.1 | Left | 106 | 20 | 13.9 | 4 | 10 | 19 |
5 | Unknown | 0 | 1 | 8.1 | 7.1 | Right | 115 | 18 | 9.9 | 5 | 10 | 19 |
6 | Unknown | 0 | 3 | 14.7 | 11.7 | Right | 98 | 23 | 8.3 | 6 | 5 | 24 |
7 | Unknown | 0 | 4 | 10.1 | 6.1 | Right | 91 | 25 | 14.9 | 7 | 5 | 25 |
Median | - | 0 | 0 | 6.1 | 6.1 | - | 95 | 18 | 13.6 | Median | 10 | 19 |
CI patients with early childhood onset, progressive deafness (Group B) | ||||||||||||
1 | Unknown | 0 | 16 | 19.8 | 3.8 | Right | 100 | 37 | 17.2 | 1 | 10 | 34 |
2 | EVA | 1 | 9 | 16.5 | 7.5 | Left | 103 | 26 | 9.5 | 2 | 12 | 26 |
3 | Unknown | 2 | 12 | 13.8 | 1.8 | Right | 91 | 17 | 3.2 | 3 | 5 | 18 |
4 | EVA | 0 | 17 | 18.2 | 1.2 | Right | 98 | 19 | 0.8 | 4 | 10 | 19 |
5 | EVA | 0 | 16 | 16.6 | 0.6 | Left | 107 | 19 | 2.4 | 5 | 5 | 19 |
6 | EVA | 0 | 12 | 14.9 | 2.9 | Right | 88 | 18 | 3.1 | 6 | 10 | 18 |
Median | - | 0 | 14 | 16.55 | 2.35 | - | 99 | 19 | 3.15 | Median | 10 | 19 |
CI patients with adult-onset deafness (Group C) | ||||||||||||
1 | Unknown | 28 | 43 | 55.0 | 12.0 | Right | 87 | 55.2 | 0.2 | 1 | 16 | 60 |
2 | Unknown | 57 | 70 | 72.6 | 2.6 | Right | 78 | 72.9 | 0.3 | 2 | 18 | 70 |
3 | Unknown | 31 | 45 | 50.1 | 5.1 | Right | 110 | 50.3 | 0.2 | 3 | 15 | 51 |
4 | Unknown | 51 | 60 | 72.1 | 12.1 | Left | 80 | 72.3 | 0.2 | 4 | 16 | 69 |
5 | Unknown | 33 | 40 | 53.9 | 13.9 | Right | 91 | 54.1 | 0.2 | 5 | 15 | 51 |
6 | Unknown | 32 | 37 | 55.0 | 18.0 | Left | 91 | 55.3 | 0.3 | 6 | 16 | 60 |
7 | Unknown | 33 | 51 | 53.1 | 2.1 | Right | 106 | 53.3 | 0.2 | 7 | 15 | 53 |
8 | Unknown | 14 | 28 | 33.9 | 5.9 | Right | 80 | 34.2 | 0.3 | 8 | 5 | 36 |
9 | Unknown | 72 | 79 | 79.5 | 0.5 | Right | 80 | 79.7 | 0.2 | 9 | 20 | 76 |
10 | Unknown | 26 | 37 | 38.1 | 1.1 | Left | 111 | 38.4 | 0.3 | 10 | 8 | 46 |
11 | Unknown | 35 | 38 | 46.2 | 8.2 | Right | 106 | 46.5 | 0.3 | 11 | 5 | 44 |
12 | S-SNHL | 55 | 55 | 62.6 | 7.6 | Left | 120 | 62.8 | 0.2 | 12 | 13 | 63 |
Median | - | 33 | 44 | 54.45 | 6.75 | - | 91 | 54.65 | 0.2 | Median | 15 | 56.5 |
The PTA data of control participants are for better hearing ear. CI, cochlear implant; HL, hearing loss; CAEP, cortical auditory evoked potential; PTA, pure tone average; EVA, enlarged vestibular aqueduct; S-SNHL, sudden sensorineural hearing loss
The latencies of P1, N1, and P2 of CAEPs in adult patients with cochlear implants (CIs) and control participants with normal hearing
Group | n | P1 latency (ms) | N1 latency (ms) | P2 latency (ms) |
---|---|---|---|---|
Prelingual deafness with CI | 7 | 70.4±10.4 | 121.5±11.4 | 184.7±20.5 |
Early childhood-onset, progressive deafness with CI | 6 | 71.5±14.0 | 125.8±14.3 | 185.3±10.2 |
Adult-onset deafness with CI | 12 | 59.9±10.5 | 113.3±18.1 | 179.5±22.4 |
Normal hearing | 25 | 53.7±7.0 | 98.3±6.8 | 162.9±15.1 |
The data are presented as mean±standard deviation