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ORIGINAL ARTICLE
Year : 2019  |  Volume : 25  |  Issue : 2  |  Page : 103-107

P300 as a measure of auditory memory in cochlear implant recipients: A preliminary report


School of Audiology and Speech Language Pathology, Bharati Vidyapeeth (Deemed to be University), Pune, Maharashtra, India

Date of Web Publication16-Aug-2019

Correspondence Address:
Dr. C S Vanaja
Department of Audiology and Speech Language Pathology, School of Audiology and Speech Language Pathology, Bharati Vidyapeeth Deemed University, Pune Satara Road, Pune - 411 043, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/indianjotol.INDIANJOTOL_118_18

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  Abstract 


Objectives: This study aimed to check the feasibility of recording autiory P300 in children with cochlear implants using commercially available auditory evoked potential system. The present study also investigated if there is an association between auditory memory and auditory P300. Methods: The participants of the study included 10 children with monaural cochlear implant attending auditory verbal therapy. The age of the children ranged from 2 years to 7 years 8 months years. Audiotry P300 was recorded using Biologic Navigator Pro Auditory Evoked Potential System. Auditory memory was measured using 4-digit sequences. Results: Cortical auditory evoked potential could be recorded from 9 out of 10 children. The latency and amplitude of P300 showed a significant correlation with memory for 4-digit sequences. Discussion: The results of the present study highlights that auditory P300 can be recorded for the passive task from children using cochlear implants. It has been reported in the literature that cognitive and memory abilities are crucial for the development of auditory discrimination and hence can be a factor affecting the outcome of cochlear implants. The results suggest that P300 can probably be used to assess memory and cognitive abilities of children using cochlear implants. Conclusions: The results suggest that P300 can be recorded in clinical setup and probably will help in the objective assessment of memory abilities in children with cochlear implants.

Keywords: Auditory memory, cochlear implant outcome, event-related potential


How to cite this article:
Vanaja C S, Sarda S. P300 as a measure of auditory memory in cochlear implant recipients: A preliminary report. Indian J Otol 2019;25:103-7

How to cite this URL:
Vanaja C S, Sarda S. P300 as a measure of auditory memory in cochlear implant recipients: A preliminary report. Indian J Otol [serial online] 2019 [cited 2019 Nov 12];25:103-7. Available from: http://www.indianjotol.org/text.asp?2019/25/2/103/264670




  Introduction Top


Cochlear implantation is a rehabilitative measure opted for persons with hearing impairment who do not benefit from hearing aids. Although a majority of persons benefit from cochlear implantation, variability exists in the outcome of cochlear implantation. Some factors affect the outcome of cochlear implantation, the variables can be broadly categorized as factors related to the subject and those related to the device. It is of utmost importance for the clinician to evaluate each of the subject-related variables to plan appropriate (re) habilitation for a child using cochlear implants. Some of subject-related factors that have been studied extensively include the age of onset of hearing loss, duration of hearing loss, age at implantation, duration of implant use, preoperative hearing thresholds, and etiology. Effect of device-related factors such as number of electrodes, type of array, speech coding strategy has also been studied. However, a review of literature shows that these factors explain only 40%–60% of the variability observed in persons with cochlear implants.[1],[2]

Pisoni et al.[3] suggested that the effectiveness of cochlear implants in children with prelingual hearing loss may depend on central auditory, cognitive, and linguistic factors. Niparko et al.[4] in their study reported that higher cortical functions such as intelligence, memory, attention, and cognitive processes might result in extreme variability in speech-language development of children with hearing impairment. It can be inferred from these reports that assessment of higher cognitive processes helps in predicting the outcome of cochlear implantation. One of the higher cognitive functions that can affect the development of speech and language is auditory memory. Different methods are used to assess memory abilities, and one among them is forward and backward digit span which is used as a measure of working memory in children with cochlear implants.[5]

While the auditory memory is best evaluated using behavioral measures, use of electrophysiological measures such as auditory evoked potentials can complement the results of behavioral measures and provide physiological evidence for the abilities measured. P300 is one of the auditory evoked potentials associated with auditory memory and cognitive abilities. It is the third positive wave of cortical auditory evoked potential elicited using oddball paradigm, generally occurring 300 ms after the presentation of the stimulus. This response is observed when a person differentiates the target stimulus from the frequently occurring train of stimuli. It is believed to reflect processes related to updating of working memory.[6] The neural generators of P300 are located in the frontal lobe, temporo-parietal junction, and hippocampus. Electrical activity resulting from the interaction between the frontal lobe and hippocampal/temporal-parietal function is reflected in the P300 wave.[7]

Conventionally, P300 is recorded using an active paradigm in which the persons being evaluated is instructed to pay attention to the target stimulus. However, P300 can also be recorded in passive condition wherein no specific instructions to attend to the stimuli are given to the participants. Studies indicate that similar auditory P300 waveforms are obtained for active tasks and passive tasks.[8],[9] The advantage of Passive P300 is that it can be recorded reliably from young children who may not understand instructions for active P300.

Initial research on P300 in recipients of cochlear implants, compared latency, and amplitude of the response recorded from persons using cochlear implant with those recorded from persons with normal hearing. Oviatt and Kileny[10] observed that the latency of P300 was longer and the amplitude was reduced in persons using cochlear implants. They further observed that the latencies were longer for difficult contrasts when compared to that of easy contrasts. It can be inferred from these findings that the latency of P300 reflects the difficulty in auditory discrimination.

P300 has been studied as an objective measure of speech perception in persons using cochlear implants. Many investigators have reported a correlation between latency of P300 and speech perception abilities. Henkin et al.[11] observed that P300 can provide information regarding the neural encoding of distinct acoustic–phonetic cues in persons using cochlear implants. Beynon et al.[12] reported that the latency and amplitude of P300 can be used to check if there is a change in perception with different speech coding strategies.

Although researchers have shown that P300 can be recorded in persons using cochlear implants, there is underutilization of this measure in clinics. One of the major reasons for underutilization is the uncertainty regarding the feasibility of recording it using the commercially available auditory evoked potential system and its clinical applications. Furthermore, to the best of the researchers' knowledge, there is a dearth of studies correlating P300 responses and auditory memory in persons using cochlear implants. Hence, we carried out a preliminary investigation to study the association between auditory memory and auditory P300 recorded from children using cochlear implants. The primary aim of the investigation was to check the feasibility of recording P300 for auditory stimuli in children with cochlear implants using a commercially available auditory evoked potential system in a clinical setup. The study also investigated the association of latency and amplitude of P300 with auditory memory in children with cochlear implants.


  Methods Top


Participants

The participants for the study included 10 children with unilateral cochlear implant attending auditory verbal therapy at Bharati Vidyapeeth Deemed University School of Audiology and Speech-Language Pathology. All the children used either Cochlear Nucleus CP 802 or CP 810 or freedom sound processor with CI 24RE (Straight/Contour Advanced) implant. Speech processing strategy was uniform across all the children. Speech processing strategy was uniform across all children. All of them used Advanced ACE speech processing strategy. The chronological age of the children ranged from 2 years to 7–8 years. Age at the time of implantation ranged from 10 months to 3 years 8 months and the duration of implant use varied from 7 months to 4 years. All the children had congenital bilateral severe to profound sensorineural hearing loss. With unilateral cochlear implant, the sound field detection thresholds were <30 dB HL from 500 to 4000 Hz for all the participants.

Procedure

Informed consent was obtained from the parents/caregivers of the children before collecting data. It was ensured that the cochlear implant device was working satisfactorily and thresholds for warble tones were obtained in the sound field set up to ensure that the thresholds are <30 dB HL from 500 Hz to 4000 Hz. The data collected for the purpose of this study included a recording of auditory P300 and assessment of auditory memory. It was ensured that all the children were able to discriminate speech sounds contrast (/ta/and/ga/) used for the recording of P300 and were able to repeat the digit the used for assessing auditory memory.

Recording of P300

P300 was recorded for auditory stimulus. Natural speech sounds/ta/and/ga/, spoken by a native Marathi speaker was recorded in a computer using adobe audition software, version 2.0. The sampling frequency was 48,000 Hz with 16-bit resolution. The duration of the stimulus was approximately 350 msec. The recorded stimulus was loaded into biologic auditory evoked potential system for recording P300.

Biologic auditory evoked potential system (Navigator pro) with auditory evoked potential software version 7.0.0 was used to record P300 using passive paradigm. Participants were seated on a chair in relaxed and comfortable position. Recordings were carried out when the participants were awake. The participants were shown a picture book or a video to ensure that they are awake but quiet. Silver coated disc electrodes were placed on testing sites after cleaning the site with skin preparing the gel. Ten-20 conduction paste was used to increase the conductivity of the signal. The electrodes were securely placed using medical tape. The inverting electrode was placed on the mastoid of the ear contralateral to the ear with cochlear implant (contralateral mastoid was chosen to reduce electrical artifacts that may arise from the cochlear implant); non-inverting electrode was placed on the vertex (Cz), and the common electrode was placed on the low forehead (Fpz). It was ensured that the electrode impedance was <5 kΩ at all the sites and the inter-electrode impedance was 2 kΩ.

Passive P300 responses were recorded using the protocol given in [Table 1]. Responses were recorded twice to ensure replicability and the waveforms obtained in two recordings were then added to improve the morphology. P1, N1, P2, N2 peaks, and P300 responses were marked independently by two audiologists who were unaware about the test conditions.
Table 1: Protocol for cortical auditory evoked potential recording

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Assessment of auditory memory

The stimuli consisted of ten tokens of randomly sequenced digits (from 1 to 10) in Marathi. Each token consisted of 4-digit sequences. Participants responded by verbally repeating the digits. Before initiating the test, it was ensured that the participants were familiar with all the digits and they were able to repeat the words. A score of one was given to a token if all the digits in the token were repeated in the correct sequence. No score was given if any of the digits were missed or not repeated in sequence. A total number of sequences correctly repeated were calculated. The obtained data were analyzed to investigate the aims of the study.


  Results Top


Cortical evoked potentials could be recorded from nine out of 10 children using cochlear implants. Cortical auditory evoked potentials could not be identified in one child due to a large number of artifacts. Among the nine participants with replicable cortical auditory evoked potentials, P300 waveform could be identified in six children and was absent in three participants. [Figure 1] shows a sample of P300 waveform obtained from one of the participants. The latency of the P300 response ranged from 337 to 560 ms whereas the amplitude varied from 0.31 to 15.42 μV. On the auditory memory test, it was observed that three children obtained a score zero.
Figure 1: P300 waveform of one of the participants (upper two waveforms represent cortical evoked potentials for frequent stimulus/ta/and lower two waveforms represent response to rare occurring stimulus/ga/)

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[Table 2] shows the chronological age, duration of cochlear implant use, scores on auditory memory test, and results of P300 waveforms for all the nine participants. It can be observed from table that all three children with absent P300 had poor auditory memory, with a score of zero. The chronological age and duration of implant use varied. Further inspection [Table 2] indicates that chronological age or the duration of implant use did not show any trend with the amplitude or latency of P300 response even in the other six children.
Table 2: Results of P300 and auditory memory for all the participants

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Pearson product moment correlation analysis was carried out to investigate if latency or amplitude of P300 response showed any association with age of the participant, age at the time of implantation, duration of implant use, and/or auditory memory. The results of the analysis are given in [Table 3]. It can be observed from the table that only auditory memory showed a significant correlation with amplitude and latency of P300. The correlation coefficient was positive for the amplitude of P300, whereas it was negative for the latency of P300 response.
Table 3: Results of Pearson product moment correlation analysis

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  Discussion Top


The results of the present study indicate that P300 waveforms for acoustic stimuli can be recorded from children using cochlear implants. It appears to be a clinically viable test as these waveforms could be recorded using a commercially available auditory evoked potential system. P300 can be used as a useful clinical tool to assess memory and cognitive functions in children using cochlear implants. There is a significant increase in number of children with complex needs receiving cochlear implants.[13] Many a times, the cognitive problems in children with hearing impairment may not be identified before cochlear implantation. It becomes imperative to test for associated/additional problems when expected improvement is not seen in children with cochlear implants. Physiological tests such as auditory P300 may become the choice of assessment in children who cannot be assessed using behavioral tests where a child may not be able to give a voluntary response. Kileny et al.,[14] reported that recording of cognitive evoked potentials in children with cochlear implants is feasible and informative. The results of the present study support these findings. Furthermore, the present study shows that P300 can be reliably recorded for the passive task from children, thus making it easy to record from those who may not follow instructions for testing.

Further the study aimed at investigating if there is an association between auditory memory and P300. A review of the literature shows that a number of factors which can have an effect on the latency and amplitude of P300. The present study included a small sample and a heterogenous sample in terms of chronological age, age at the time of implantation, and the duration of implant use. The age of the participants varied from 2 year to 7 years 8 months and the duration of implant use varied from 7 months to 4 years. Tsai et al.,[15] reported that latency of P300 of children in the age range of 6–7 years was significantly longer than older children. They further reported that there is no significant increase in latency of P300 in children in the age range of 8–13 years. Various studies have reported a slope of P300 latency varies from 3.6 to 18.4 ms/year.[16],[17] Pearson product moment correlation revealed that chronological age, duration of implant use, or age at the time of implantation did not show any significant correlation latency or amplitude of P300. Inspection of the data shows a decreasing trend in latency of P300 with an increase in age. Probably, statistical significance was not observed as the sample size was too small.

Auditory memory span showed a significant correlation with the latency and amplitude of P300. Correlation analysis revealed that with an increase in memory scores, there was a significant increase in the amplitude of P300 and a significant decrease in the latency of P300. The results need to be interpreted with caution as many of the factors which can have an effect on P300 response were not controlled and the sample size was small. However, these results are in consonance with an earlier hypothesis that auditory P300 reflects auditory memory[6] and can be used to assess high-level processing in children who cannot be tested behaviorally. It has also been reported that auditory memory can affect speech perception[18] which, in turn, can influence the development of speech and language in children with cochlear implants. Harris et al.,[19] reported that neurocognitive factors underlying information processing can explain some of the variability in speech language acquisition of children with cochlear implants. They further observed that measured of short term verbal memory and word memory predicted long-term speech language outcomes. Hence probably recording P300 can help in predicting speech language outcomes in children.

Kronenberger et al.[20] reported that children with profound deafness who receive a cochlear implant had a higher risk of having delays in areas of working memory, controlled attention, planning, and conceptual learning when compared to age-matched normal hearing children. Pisoni et al.,[21] observed that immediate verbal-phonological short-term memory, assessed with Digits Forward, to be strongly related to speech-language outcomes. They recommended that there is a need to identify the core neurocognitive processes that underlie development of speech and language functioning in children with cochlear implants. The present study showed a significant correlation between auditory memory assessed using digit forward sequence and P300 response. Hence, it is recommended that the recording of P300 be included in the test battery to assess neurocognitive processes as it is an electrophysiological response that can be elicited without any voluntary response from the participant.


  Conclusions Top


The presence of P300 for a passive task in young children using cochlear implants encourages the recording of P300 in clinical settings. A significant correlation between auditory memory and P300 suggests that recording of P300 may help in assessing memory in difficult to test population.

Acknowledgments

The authors would like to thank the members of Cochlear Implant unit of BVDU SASLP, Dr. Gauri Belsare, ENT surgeon and Principal of BVDU SASLP, Prajakata Nalat, Assist Professor, Trupti Bhave, Auditory Verbal Therapist.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Tobey EA, Geers AE, Douek BM, Perrin J, Skellet R, Brenner C, et al. Factors associated with speech intelligibility in children with cochlear implants. Ann Otol Rhinol Laryngol Suppl 2000;185:28-30.  Back to cited text no. 1
    
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3.
Pisoni DB, Cleary M, Geers AE, Tobey EA. Individual differences in effectiveness of cochlear implants in children who are prelingually deaf: New process measures of performance. Volta Rev 1999;101:111-64.  Back to cited text no. 3
    
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Niparko JK, Tobey EA, Thal DJ, Eisenberg LS, Wang NY, Quittner AL, et al. Spoken language development in children following cochlear implantation. JAMA 2010;303:1498-506.  Back to cited text no. 4
    
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Pisoni DB, Cleary M. Measures of working memory span and verbal rehearsal speed in deaf children after cochlear implantation. Ear Hear 2003;24:106S-20S.  Back to cited text no. 5
    
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Goldstein A, Spencer KM, Donchin E. The influence of stimulus deviance and novelty on the P300 and novelty P3. Psychophysiology 2002;39:781-90.  Back to cited text no. 6
    
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Huang WJ, Chen WW, Zhang X. The neurophysiology ofP300 – An integrated review. Eur Rev Med Pharmacol Sci 2015;19:1480-8.  Back to cited text no. 7
    
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Oviatt DL, Kileny PR. Auditory event-related potentials elicited from cochlear implant recipients and hearing subjects. Am J Audiol 1991;1:48-55.  Back to cited text no. 10
    
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Nittrouer S, Caldwell-Tarr A, Lowenstein JH. Working memory in children with cochlear implants: Problems are in storage, not processing. Int J Pediatr Otorhinolaryngol 2013;77:1886-98.  Back to cited text no. 18
    
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Harris MS, Kronenberger WG, Gao S, Hoen HM, Miyamoto RT, Pisoni DB, et al. Verbal short-term memory development and spoken language outcomes in deaf children with cochlear implants. Ear Hear 2013;34:179-92.  Back to cited text no. 19
    
20.
Kronenberger WG, Beer J, Castellanos I, Pisoni DB, Miyamoto RT. Neurocognitive risk in children with cochlear implants. JAMA Otolaryngol Head Neck Surg 2014;140:608-15.  Back to cited text no. 20
    
21.
Pisoni DB, Kronenberger WG, Roman AS, Geers AE. Measures of digit span and verbal rehearsal speed in deaf children after more than 10 years of cochlear implantation. Ear Hear 2011;32:60S-74S.  Back to cited text no. 21
    


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