Cortical maturation in children with cochlear implants: Correlation between electrophysiological and behavioral measurement

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Central auditory pathway maturation in children depends on auditory sensory stimulation. The objective of the
resent study was to monitor the cortical maturation of children with cochlear implants using electrophysiological and auditory skills measurements. The study was longitudinal and consisted of 30 subjects, 15 (8 girls and 7 boys) of whom had a cochlear implant, with a mean age at activation time of 36.4 months (minimum, 17 months; maximum, 66 months), and 15 of whom were normal-hearing children who were matched based on gender and chronological age. The auditory and speech skills of the children with cochlear implants were evaluated using GASP, IT-MAIS and MUSS
easures. Both groups underwent electrophysiological evaluation using long-latency auditory evoked potentials.

Each child was evaluated at three and nine months after cochlear implant activation, with the same time interval adopted for the hearing children. The results showed improvements in auditory and speech skills as measured by IT-MAIS and MUSS. Similarly, the long-latency auditory evoked potential evaluation revealed a decrease in P1 component latency; however, the latency remained significantly longer than that of the hearing children, even after nine months of cochlear implant use. It was observed that a shorter P1 latency corresponded to more evident development of uditory skills.

Regarding auditory behavior, it was observed that children who could master the auditory skill of discrimination showed better results in other evaluations, both behavioral and electrophysiological, than those who had mastered only the speech-detection skill. Therefore, cochlear implant auditory stimulation facilitated auditory pathway maturation, which decreased the latency of the P1 component and advanced the development of auditory and speech skills. The analysis of the longlatency auditory evoked potentials revealed that the P1 component was an important biomarker of auditory development during the rehabilitation process.

Hearing loss is an impairment that impedes full reception of the acoustic signal by the auditory cortex because it reduces stimulation of the auditory pathways. In childhood, severe or profound, hearing loss affects the evelopment or maintenance of oral language and, consequently, the individual’s relationships and lifestyle [1,2]. Cochlear implants (CI) are an important clinical resource for children with hearing loss who do not show significant results in auditory skill development with the use of only a hearing aid [3]. This electronic device is meant to partially replace the sensory function of the cochlea through direct electrical stimulation of the auditory nerve fibers, which allows access to speech sounds and thereby improves the quality of life of these patients [4,5]. Auditory stimulation during childhood allows the central auditory nervous system (CANS) to undergo changes and
eorganization, called neuronal plasticity, that facilitate the development of auditory skills (detection,
iscrimination, recognition and comprehension) that are necessary for oral language development [6±13]. However, the behavioral auditory and language response after CI activation is not always immediate and precise because progress is gradual and results can be influenced by many variables, such as sensory deprivation time, age at activation, degree and type of hearing loss, acquisition time (pre- or post-lingual), etiology, the presence of residual hearing, speech therapy, family motivation and involvement, and the presence of other comorbidities that can affect the maturation process (syndromes or delays in general psychomotor development) [14]. Furthermore, optimization of the CI’s benefit does not depend only on these variables or on the electrical signal generated by the device. The integrity of the central auditory pathways that carry sound information to the primary auditory cortex (located in Heschl’s gyrus) and the ability of other associated areas, such as the secondary auditory area (which extends to the lateral surface of the temporal lobe) and Wernicke’s area (which includes part of the temporal plane and posterior superior part of the first temporal gyrus), can significantly affect optimization; both factors are related to auditory learning and allow the CI user to add meaning to acoustic signals [15,16]. The existence of a sensitive period for early stimulation aiming for a greater CI benefit is discussed in the literature, and in general, the consensus is that up to three years of age is the perfect time to start the process of re)habilitation [17,18,19]. After this sensitive period, abnormalities in the development of synaptic plasticity occur, resulting in abnormal neuronal connectivity among cells, as well as disintegration and functional immaturity of auditory cortical areas [11,12,18]. Thus, the feedback between the primary and secondary auditory areas is impaired, and some auditory areas can develop non-auditory functions such as visual and somatosensory functions, a
phenomenon called cross-modal plasticity [17,20±26].

To evaluate the development of auditory and language skills, specific protocols are used and should be selected according to the child’s age and developmental level. Besides that, questionnaires should be given to parents or guardians to provide quantitative and qualitative feedback regarding the child’s performance in daily life
27,28,29]. Considering the subjective nature of behavioral measures, evaluation by means of longlatency auditory evoked potentials (LLAEPs) has recently emerged as a way to objectively evaluate the benefits provided by the CI to complement behavioral evaluation. This test can measure the degree of development and plasticity limits of central auditory pathways by analyzing changes in the morphology and P1 component latencies present in this potential [11,18,26,30± 35], generated by the electrical activity of the primary auditory cortex and associated thalamic
regions [12]. Therefore, the evaluation of LLAEPs in conjunction with behavioral auditory and language measurements could be valid for monitoring the development of auditory and oral Cortical maturation with the cochlear implant
PLOS ONE | DOI:10.1371/journal.pone.0171177 February 2, 2017 2 / 18 language skills in hearing-impaired children after the intervention and could therefore help to establish treatment guidelines [18,19,32,34,36±43].

However, studies that determine the correlation between behavioral auditory and language measurements and
lectrophysiological evaluations are still insufficient for LLAEP evaluations to be used in clinical practice, particularly in patients who are difficult to evaluate using behavioral measures, for reasons of age, restricted auditory experience or any other factor related to cognition and development. Despite several studies in recent decades that have aimed to characterize LLAEP findings in children with CI, the heterogeneity of this population makes it difficult to establish a consensus on what to expect from electrophysiological results after CI ctivation. The objective of the present study was to monitor the cortical maturation of children with CI by means of electrophysiological and auditory and speech skills measurements.