Cortical Neuroplasticity Across Auditory, Visual, and Somatosensory Modalities in Children with Cochlear Implants

Auditory deprivation, as in hearing loss, appears to tax the brain, resulting in changes in cortical resource allocation. One form of cortical resource allocation in hearing loss is crossmodal reorganization, whereby cortical resources in the deprived modality are recruited and repurposed for processing by other sensory modalities. Cross-modal reorganization has been proposed as a source of variability underlying speech perception in patients receiving cochlear implants (CIs). Previous studies have documented cross-modal recruitment of auditory cortex for visual and somatosensory processing in hearing-impaired children with CIs. However, changes within the auditory modality have not been documented alongside visual and somatosensory cross-modal changes within the same subject group. Thus, the goal of this study was to examine cross modal reorganization across all three sensory modalities within a single group of CI children (n = 10) using high-density EEG. Behavioral correlates of speech perception in background noise were also measured. Amplitude and latency of cortical auditory, visual, and somatosensory evoked potentials were analyzed and source localization was performed to visualize cortical activation patterns within the entire group of CI children, and across groups of CI children exhibiting good vs. poor speech perception. Results suggest widespread changes in cortical resource allocation in CI children in all three sensory modalities. Further, frontal cortex activation was observed in response to auditory and visual stimulation in CI children, suggesting that frontal areas may be recruited as a means to help compensate in speech perception and/or higher-order cognitive processing tasks. CI children with good speech perception did not show recruitment of frontal cortex or cross-modal recruitment by visual processing, while the children with poor speech perception did. Taken together, results of this study reflect CORTICAL NEUROPLASTICITY IN CHILDREN WITH COCHLEAR IMPLANTS 3 widespread changes in cortical networks in CI children, and it appears that these changes are correlated with functional performance. CORTICAL NEUROPLASTICITY IN CHILDREN WITH COCHLEAR IMPLANTS 4 Cortical Neuroplasticity Across Auditory, Visual, and Somatosensory Modalities in Children with Cochlear Implants For the significant portion of the population with a severe or profound hearing loss, the most viable treatment option is a cochlear implant (CI). While treatment with CIs has proven successful, the variability of success among those treated remains high. Research on neural changes associated with hearing loss and its treatment may explain this variability and is therefore critical to improving rehabilitation in the hearing-impaired population. A basic tenet of neuroplasticity is that that the brain will reorganize when it is deprived of sensory input. The present study attempts to understand how treatment of deaf children with CIs affects brain reorganization across sensory modalities: vision, audition (hearing), and somatosensation (touch). Furthermore, in an effort to determine whether the brain’s reorganization is associated with better or poorer outcomes with CIs, these neural changes were compared to a behavioral test of speech perception in noise. This comparison helps establish whether the neuroplastic changes occurring are adaptive (helpful in speech perception) or maladaptive (negatively affects speech perception) for children with CIs. Literature Review Neural plasticity is a phenomenon that allows us to interact with, adapt to, and learn from environments and experiences. The brain’s ability to reorganize when it is deprived of sensory input is just one example of neural plasticity, but has been key to studying the malleability of cortical connections. This phenomenon, known as cross-modal reorganization or cross-modal plasticity, has been demonstrated in studies of the congenitally deaf populations— such studies have shown that the deprived auditory cortex is subject to recruitment by the CORTICAL NEUROPLASTICITY IN CHILDREN WITH COCHLEAR IMPLANTS 5 visual system for visual perception in both humans and animals (Neville & Lawson, 1987; Sharma & Mitchell, 2013; Finney, Fine, & Dobkins, 2001; Finney, Clementz, Hickok, & Dobkins, 2003; Lomber, Meredith, & Kral, 2010). In addition to recruitment of auditory cortices by vision, deaf populations have also been found to demonstrate recruitment by the somatosensory modality (Levänen and Hamdorf, 2001). Essentially, some higher-order cortical areas that would be used for auditory processing in animals and humans with normal hearing were found to process different stimuli in those who experience hearing loss. Cortical reorganization that occurs with sensory deprivation affects behavioral outcomes in that cross-modal plasticity tends to be beneficial for the recruiting modality. For example, Lomber et al. (2010) found that congenitally deaf cats had improved visual capabilities such as localization in the periphery and movement detection. However, reversible deactivation of the dorsal and posterior auditory cortices eliminated these superior visual abilities. It was therefore concluded that the supranormal visual performance in the deaf cats was subserved by cross-modal recruitment of deprived auditory cortex. The visual benefits of cross-modal recruitment have also been documented in deaf humans who demonstrate improved visual motion detection (Hauthal, Sandmann, Debener, & Thome, 2013). However, the effects of hearing loss are not limited only to changes in sensory cortices of the brain. In comparison to normal-hearing (NH) controls, adults with mild to moderate hearing loss have shown recruitment of frontal cortices for processing of auditory stimuli (Campbell & Sharma, 2013; Sharma et al., 2016). The activation of the frontal and pre-frontal cortex, areas traditionally associated with executive function and working memory, implies changes in cortical resource allocation due to increased listening effort in age-related hearing loss. Frontal areas may be CORTICAL NEUROPLASTICITY IN CHILDREN WITH COCHLEAR IMPLANTS 6 recruited as a means to help compensate in speech perception and/or higher-order cognitive processing tasks. Thus, two forms of compensatory neuroplasticity have been demonstrated by populations with hearing loss: cross-modal reorganization and changes in cortical resource allocation such as frontal activation. While cross-modal plasticity is well documented in deaf populations, fewer studies have been done on its occurrence in populations who have received treatment for hearing loss. Cochlear implantation remains the leading treatment for people with severe to profound hearing losses; it is estimated that over 400,000 people world-wide have received CIs (NIDCD, 2012). By directly stimulating the auditory nerve, the implant is able to transmit an electrical representation of acoustic signals which the brain interprets and processes as sound. The development of the CI has been key to the scientific exploration of neural plasticity for two reasons: first, it enables the study of neuroplastic changes induced by deprivation, and second, it has allowed the auditory system to become a model system due to convergence between animal and human data (Kral, Hartmann, Tillein, Heid, & Klinke, 2002). Studies have shown that the plasticity induced by cochlear implantation is optimized by early implantation within a critical period (Kral & Sharma, 2012); however, even those implanted within this period show significant variability of language outcomes (Kral, Kronenberger, Pisoni, & O’Donoghue, 2016). One example of cross-modal reorganization in populations with CIs was documented by Campbell & Sharma in a group of twelve children (2016). Current density reconstruction (CDR) was used to calculate the probable cortical activation sources of children’s responses to a visual motion stimulus. The resulting source reconstruction revealed that the NH control group showed activation of visual motion processing areas (cerebellum, striate, extrastriate) while CI CORTICAL NEUROPLASTICITY IN CHILDREN WITH COCHLEAR IMPLANTS 7 children showed activation of both visual areas and auditory areas (inferior, middle, and superior temporal gyrus). This finding suggests that in children with CIs, auditory cortical areas were recruited by vision via cross-modal plasticity. Cardon (2015) also provided evidence for recruitment of auditory areas by the somatosensory modality. Similar methodology revealed that, as expected, a vibrotactile stimulus evoked activation of the contralateral somatosensory cortex (pre/post-central gyrus) in NH children. The CI group, however, showed activation of both contralateral somatosensory and contralateral auditory cortices (inferior, middle, and superior temporal gyrus). This finding suggests that the deprived auditory cortical areas were recruited by the somatosensory modality for the processing of a vibrotactile stimulus, another example of cross-modal plasticity in children with CIs. The existing literature would suggest that vision, audition, and somatosensation are flexible, interrelated processes where a change in input in one modality will result in the potential reorganization of the brain for neuronal processing of the other two. The above studies of both Campbell & Sharma and Cardon have each surveyed cross-modal recruitment by a single modality (vision and somatosensation, respectively) but have failed to assess the brain’s responses across visual, somatosensory, and auditory modalities within the same group of CI subjects. Through neurophysiological testing of auditory, visual, and somatosensory processing and comparative behavioral assessments, the present study attempts to draw conclusions about how cross-modal plasticity occurs among all three modalities for ten children with CIs. CORTICAL NEUROPLASTICITY IN CHILDREN WITH COCHLEAR IMPLANTS 8 Methods Parti