April 14, 2009 Features

Brain Maturation in Children With Cochlear Implants

Over the last several decades, neuroscience has provided new information about critical periods for brain maturation, characteristics of plasticity in a maturing brain, factors that affect central auditory pathways, and cortical re-organization that can occur when stimulation patterns differ from the norm. This information can be useful to audiologists and speech-language pathologists who work with children who have severe-to-profound hearing loss and receive intervention with cochlear implants and/or hearing aids.

The five questions below address the main aspects of our recent research on cortical plasticity and development in children with congenital deafness and the work of other scientists in that area.

When is the best time to provide a cochlear implant (CI) to a young child with congenital deafness?

It is well known that there are critical periods for neurobiological development in the brain. A sensitive period for the development of the central auditory system is a time when the central auditory pathways have the greatest plasticity (or responsiveness), and are primed for stimulation-driven development. It is reasonable to believe that cochlear implantation occurring within this sensitive period would achieve the most positive results.

One objective measure of the development of auditory cortical pathways is the latency (timing) of cortical auditory-evoked potentials (CAEPs). In particular, the latency of the first positive peak (P1) of the CAEP in children is considered an indicator, or biomarker, of the mature development in the auditory cortical areas. The P1 peak latency varies as a function of age—and is considered an index of cortical auditory maturation.

Evidence from intracranial recordings in humans, as well as from animal models, suggests that several generators of the P1 CAEP are within the auditory cortex. Our team has established a normal range for the latency of the P1 waveform peak at different ages (Sharma et al., 2002a), with generally higher peak latency in newborns and a decrease thereafter. A newborn may have a P1 peak latency of around 300 ms. Rapid development during the first two to three years leads to a rapid decrease in P1 latency—3-year-olds have a P1 latency of about 125 ms. Adults have a P1 latency of around 60 ms. Information about the normal development of the P1 CAEP biomarker allows us to assess children with hearing loss, to determine whether they are developmentally "on track" in terms of neural processing of auditory information.

The P1 response has been measured in children who are deaf and who received cochlear implants at different ages to examine the limits of plasticity in the central auditory system (Ponton et al., 1996; Sharma & Dorman, 2006). We examined P1 latency in 245 children with congenital deafness who were fit with a CI, and reported that children who received CI stimulation early in childhood (< 3.5 years) had normal P1 latencies, but children who received CI stimulation late in childhood (> 7 years) had abnormal cortical response latencies (Sharma et al., 2006). A group of children receiving CIs between 3.5 and 7 years revealed highly variable response latencies. In general, for the majority of children who were implanted after age 7 years, response latencies did not reach normal limits even after several years of experience with the implant.

Overall, our P1 data suggest that the most optimal period for central auditory development is during the first 3.5 years of life. There is some variability in the data between the ages of 3.5 to 7 years. However, in all likelihood, the sensitive period ends at age 7. This finding of a sensitive period for central auditory development in humans is consistent with studies in animals that have shown a sensitive period for auditory cortical development (Kral et al., 2002). These findings also correspond to previous research that shows that children with congenital deafness who are younger than age 4 and receive a cochlear implant develop significantly better speech and language compared to children who receive implants after 6–7 years of age (Kirk et al., 2002).

What happens at the end of the sensitive period, if little or no auditory stimulation is provided to the brain?

Studies with cats with congenital deafness have established a possible mechanism for the end of the sensitive period. When electrical stimulation is started after four to five months of deafness—after the end of the sensitive period in cats for central auditory development—there is a delay in the activation of superficial supragranular) layers of the cortex and almost no activity at longer latencies and in deeper (infragranular) layers (Kral, Tillein, Heid, Hartmann, & Klinke, 2005). The near-absence of activity in deeper layers suggests incomplete development of inhibitory synapses and an altered information flow from deeper to superficial layers. The higher-order auditory cortex projects back to the primary auditory cortex, mainly to the deeper layers; these layers (V & VI) send long-range feedback projections to the subcortical auditory areas.

The absence of activity in deeper layers can be interpreted to suggest a functional decoupling of primary cortex from the higher-order auditory cortex, also affecting feedback projections to subcortical auditory structures (Kral et al., 2000; Kral et al., 2002; Kral et al., 2005). That is, with a lack of typical auditory experience, activity in the deeper layers of the cortex is severely compromised. Projections do not develop properly from secondary auditory areas back to the primary auditory areas, and these important feedback loops are weakened.

At the end of the sensitive period, therefore, the secondary auditory areas may be completely or partially decoupled from primary auditory areas, and are no longer able to provide important cognitive, "top-down" modulation (Kral & Eggermont, 2007). The decoupling of primary and secondary auditory areas may actually make the secondary areas more available to other modalities, such as vision, in the process of re-organization. Kral (2007) cites these mechanisms to explain why auditory processing becomes difficult after the sensitive period. Specifically, modulation of the primary auditory areas is changed, affecting plasticity, and cortical areas important for auditory and linguistic processing are re-purposed by other systems. These changes make efficient analysis a challenge for any new incoming auditory stimuli.

How does a child's auditory cortex re-organize after long period of auditory deprivation?

Gilley, Sharma, and Dorman (2008) used high-density EEG measures to document the areas of activation (in response to a speech sound) in the brains of children with normal hearing and age-matched children who received CIs before 3.5 years of age and after 7 years of age (i.e., before and after the sensitive period age cut-offs). As expected, children with normal hearing showed bilateral activation of the auditory cortical areas (superior temporal sulcus and inferior temporal gyrus). As shown in Figure 1 [PDF] children who received CIs at an early age (<3.5 years of age) showed activation of the auditory cortical areas contralateral to their CI, closely resembling that of subjects with normal hearing. However, late-implanted children (>7 years of age) showed activation outside the auditory cortical areas (in the visual, insula, and parietotemporal areas).

Gilley, Sharma, and Dorman (2008) suggest that absence (or partial absence) of auditory cortical activity in late-implanted children (as shown in Figure 1 [PDF]) is consistent with Kral's decoupling hypothesis, suggesting that disconnection between the primary and higher-order cortex underlies the end of the sensitive period in cats with congenital deafness, and presumably, in late-implanted children with congenital deafness.

Can other modalities, such as vision or touch, re-wire portion of the auditory cortex after long periods of auditory deprivation in individuals who are deaf?

Partial or complete decoupling of the primary and secondary cortices leaves the secondary cortex open to re-organization by other sensory modalities. There is clear evidence of visual and touch (somatosensory) activation of the higher-order auditory cortex, also known as cross-modal reorganization, described in the seminal work of Helen Neville and colleagues (for a review, see Bavelier & Neville, 2002) as well as recent neuroimaging studies (Fine et al., 2005; Finney et al., 2003; Finney et al., 2001; Sharma et al., 2007). For example, Fine et al. (2005) used functional magnetic resonance imaging (fMRI) to assess activation patterns in response to visual stimuli in three groups: people with normal hearing and fluency in American Sign Language (ASL), people with normal hearing who do not sign, and people who are deaf who use ASL.

Visual stimuli activated areas within the auditory cortices of ASL users who were deaf; those areas were not activated in subjects with normal hearing (signing or non-signing). No difference was found between deaf and hearing participants in activation or attention modulation in the visual cortex. Because activation of the auditory cortex in response to visual stimuli was limited to participants who were deaf, researchers suggest that the effects they measured were driven by auditory deprivation rather than exposure to sign language. Attention to visual stimuli increased the activation of the auditory cortex in participants who were deaf, suggesting input from higher-level association areas, consistent with the decoupling hypothesis of Kral and colleagues.

In another study (Sharma et al., 2007), magnetoencephalographic (MEG) brain activity was recorded in an adult with normal hearing and an adult who was deaf during vibrotactile stimulation to the hand. Brain-source analysis of the averaged evoked potentials showed bilateral activation of the somatosensory cortex in the adult with normal hearing. However, in response to vibrotactile stimulation, the adult who was deaf showed bilateral activation in the somatosensory cortex and in the posterior regions of the superior temporal sulci, including Wernieke's area (areas that would usually process auditory information, including oral language). That is, in the adult who was deaf, vibrotactile stimuli that would usually activate the somatosensory cortex also activated areas of the higher-order auditory cortex.

Results of these studies suggest that at least some cross-modal plasticity and reorganization is likely among visual, somatosensory, and auditory areas after prolonged periods of auditory deprivation.

How can audiologists apply clinical biomarkers of cortical and plasticity in their work?

Our longitudinal studies of nearly 1,000 children with normal hearing, hearing aids, and CIs have revealed patterns in the CAEP waveform that are reasonably easy to identify and are predictive of abnormalities in central auditory maturation (Sharma & Dorman, 2006). Using the P1 CAEP as a clinical biomarker to track the maturation of the central auditory pathways may be a useful clinical tool in the assessment of children with hearing loss. The P1 biomarker may be considered one indicator of a plastic neural system, which may be used to provide supplementary information as part of a comprehensive audiological battery.

The morphology of the CAEP typically reflects the maturational status of the central pathways prior to intervention (Sharma & Dorman, 2006). After infants and young children with hearing loss are appropriately stimulated with either acoustic or electrical stimulation, distinct changes in CAEP waveform morphology and latency occur, indicating progress in central auditory development.

Although there is some potential clinical value of the P1 CAEP, serious issues must be considered. The age, hearing history, absence of device artifact, and understanding of normal developmental patterns are vital to the success of waveform acquisition and interpretation. Clinicians attempting to perform the P1 must be well-trained and able to test and interpret their results accurately. With these caveats, the P1 CAEP may hold promise as an addition to a clinical testing repertoire for infants with hearing loss (Nash et al., 2008).

The P1 biomarker has been developed using 10 years of basic science research findings, and our studies suggest that it may have a role to play within the battery of audiological test procedures. When recorded appropriately and interpreted properly, P1 biomarker results may provide useful information regarding maturation of the central auditory pathways in children with hearing impairment. This information, when used cautiously in conjunction with other audiological, speech, and language test results, may provide clinicians with better direction as they make decisions about appropriate intervention for infants and children with hearing loss. 

Research described in this article was supported by NIH. The authors specifically wish to acknowledge the contributions of Michael Dorman, Kathryn Martin, and Phillip Gilley.

Anu Sharma, PhD, CCC-A, is professor in the Department of Speech, Language, and Hearing Sciences at the University of Colorado at Boulder, and director of the department's Brain and Behavior Laboratory. Contact her at anu.sharma@colorado.edu.

Amy Nash, MS, CCC-A, is a doctoral student in the University of Colorado at Boulder Department of Speech, Language, and Hearing Sciences and a research audiologist in the Brain and Behavior Laboratory. Contact her at amy.nash@colorado.edu.

cite as: Sharma, A.  & Nash, A. (2009, April 14). Brain Maturation in Children With Cochlear Implants. The ASHA Leader.

Case Studies: Two Examples

The following two examples, adapted from actual case studies, demonstrate the benefit of early intervention services and show how the clinical relevance of the P1 CAEP.

Case 1

A child with a congenital profound hearing loss was referred after failing newborn hearing screening and fitted with a hearing aid at age 18 months (Figure 2  [PDF]). He did not appear to receive much aided benefit and his P1 latency showed no sign of improvement three months after hearing aid fitting, indicating that the hearing aid was not providing adequate amplification for normal development of the central auditory pathways.

He was diagnosed with a progressive hearing loss and, as he met the criteria for cochlear implant candidacy, was fitted with a CI at age 22 months. P1 latencies, which were obtained at three-month intervals after implantation, revealed normal responses at six months post-implantation, and continued to develop normally at 12 months post-implantation. The P1 data suggest that the CI was providing the stimulation necessary for normal development of central auditory pathways not provided by the hearing aid. These P1 results were consistent with results obtained from early-implanted patients at one-year post activation, who have made considerable progress in speech and language acquisition.

Case 2

This child, diagnosed with a bilateral, moderate-to-severe hearing loss, was fitted with amplification at 11 months of age. Her P1 responses were tested at the initial hearing aid fitting and then at five, 12, and 18 months post-hearing aid fitting (Figure 3  [PDF]). Although her P1 latencies were delayed initially, the P1 response reached normal limits at five months post-hearing aid fitting. The P1 latencies continue to reflect a normal auditory developmental trajectory at later test dates. The results, which suggest that the hearing aids were providing adequate stimulation for normal development of the central auditory pathways, are consistent with behavioral evaluations that showed progress in speech and language acquisition. At the time of the P1 testing at 18 months post-hearing aid fitting, the child was not considered a cochlear implant candidate; however, it will be important to continue to monitor her progress using behavioral measures and P1 responses to ensure that she is making adequate progress in speech and language development and continuing to show normal cortical development.

The access to auditory stimulation (electric or acoustic) for these patients maintained neural plasticity and allowed for development of the central auditory pathways. It is likely that the development of early communication behaviors following early intervention may be promoted by normal development of the central auditory pathways (Sharma et al., 2004). However, although the P1 is useful as a marker of a plastic neural system, it cannot encompass the complex influences that lead to expert use of oral speech and language. 



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