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Structural neuroimaging of the altered brain stemming from pediatric and adolescent hearing loss—Scientific and clinical challenges

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Abstract There has been a spurt in structural neuroimaging studies of the effect of hearing loss on the brain. Specifically, magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI) technologies provide an opportunity to quantify changes in gray and white matter structures at the macroscopic scale. To date, there have been 32 MRI and 23 DTI studies that have analyzed structural differences accruing from pre‐ or peri‐lingual pediatric hearing loss with congenital or early onset etiology and postlingual hearing loss in pre‐to‐late adolescence. Additionally, there have been 15 prospective clinical structural neuroimaging studies of children and adolescents being evaluated for cochlear implants. The results of the 70 studies are summarized in two figures and three tables. Plastic changes in the brain are seen to be multifocal rather than diffuse, that is, differences are consistent across regions implicated in the hearing, speech and language networks regardless of modes of communication and amplification. Structures in that play an important role in cognition are affected to a lesser extent. A limitation of these studies is the emphasis on volumetric measures and on homogeneous groups of subjects with hearing loss. It is suggested that additional measures of morphometry and connectivity could contribute to a greater understanding of the effect of hearing loss on the brain. Then an interpretation of the observed macroscopic structural differences is given. This is followed by discussion of how structural imaging can be combined with functional imaging to provide biomarkers for longitudinal tracking of amplification. This article is categorized under: Developmental Biology > Developmental Processes in Health and Disease Translational, Genomic, and Systems Medicine > Translational Medicine Laboratory Methods and Technologies > Imaging
Different image modalities stratified into structural (top row) and functional (bottom row) imaging. The different contrasts at the macroscopic level of 1 mm3 provide information about three types of tissues: gray matter, white matter, and cerebrospinal fluid. An MRI scan provides a view of the highly folded cortex (shown in light grayscale) and the underlying white matter (shown in bright grayscale). The scalar modalities (FA, MD, and color map) derived from DTI scans provide different ways of looking at white matter structures. The red, green, and blue colors in the color map indicate orientation in the left–right, anterior–posterior, and superior–inferior directions, respectively. The PET and fMRI scans provide a view of responses to brain activity. CAEP and fNIRS brain activity are overlaid on MR scans for reference. Activity associated with the first positive peak in the CAEP waveform (i.e., P1) is located in the primary auditory cortex contained within the Heschl's gyrus. (Reprinted with permission from Sharma et al. (, fig. 2). Copyright 2016, Wolters Kluwer Health) Activity associated with speech is located in the superior temporal gyrus containing Heschl's gyrus and planum temporale (often called the primary and secondary auditory cortex) on both sides (Reprinted with permission from Figure b in Sevy et al. (). Copyright 2010, Elsevier). Mapping these scans to parcellated atlases provides an opportunity to perform quantitative analysis of structural and functional data in common coordinates (Miller, Faria, Oishi, & Mori, ; Miller, Younes, & Trouvé, ; Mori, Oishi, Faria, & Miller, )
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Interpretation of Kral's decoupling hypothesis (Adapted from Kral and Eggermont (, fig. 3). Copyright 2007 Elsevier) based on LCDM analysis in Figure . Similarities at smaller distances, that is, lower cortical layers may facilitate top‐down processing, that is, contextual or linguistic comprehension. This may be due to priming of the auditory pathway in childhood via amplification with hearing aids albeit at a lower rate than with cochlear implants. However, this might be compromised by larger differences at larger distances, that is, upper cortical layers which may be attributed to weaker thalamic inputs and make bottom‐down processing, that is, comprehension of phonemes comprehension difficult and complex. In turn, the inputs to the lower layers and thence the other cortical areas are weakened. Additional evidence of weaker thalamic connections may manifest in those to other cortical areas such as the parietal cortex as might be in the case in the visualization of current density reconstruction in late implanted children (lower right panel from fig. 3 in Gilley, Sharma, & Dorman (). Copyright 2008, Elsevier). This suggests that hearing loss results in two‐speed thalamic inputs (Takesian et al., ). One conjectures that amplification provided by hearing aids is weaker than that provided by cochlear implants and further that the thalamo‐parietal pathway cannot tolerate the high activity levels stemming almost immediately after activation of the cochlear implant, thus forcing the neural activity to traverse along the acoustic radiation to the Heschl's gyrus (top and middle right panels from fig. 2 in Gilley et al. ())
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Labeled cortical distance map (LCDM) histograms are normalized frequencies of distances of gray matter 1 mm3 voxels relative to gray/white cortical surfaces. Shown are individual LCDMs for the Heschl's gyrus and planum temporale in five adults with hearing loss (dashed) and five matched controls (solid lines). Horizontal and vertical scales are from −1 to 5 mm and 0.0 to 0.6, respectively. p‐Values from one‐sided Kolmogorov–Smirnov tests for the pooled cummulative distribution function (cdf) for the control subjects to be left of the pooled cdf for the subjects with hearing loss were significant for all four structures (≪.0001). For pooled LCDMs, see Ratnanather et al. ()
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Simplified schematic illustration of transmission of acoustic information from the left and right cochleae to the brain. Note information crosses over in the brainstem as well as in the cortex. Please refer to Figures and for association cortical regions such as planum temporale. The white matter connections include those between primary and associated cortical regions and those that project back to other structures via the thalamus and brainstem
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3D visualization of gray matter and white matter structures found to be different in people with hearing loss based on Table . Please refer to Figure for the possible roles these structures play in the auditory pathway. Upper left shows the lateral view of the left side of the JHU‐MNI‐SS brain (Oishi et al., ); lower right shows the lateral view of the left medial structures adjacent to the mid‐sagittal plane of the right hemi‐brain. The cortical structures (Pars Triangularis, Pars Opercularis, Motor Cortex, Superior Temporal Gyrus, Planum Temporale, Visual Cortex and Cerebellum, Heschl's Gyrus, Insula, Fusiform Gyrus) and one white matter structure (corpus callosum) were obtained from the JHU‐MNI‐SS labels and triangulated. CAWorks (www.cis.jhu.edu/software/caworks) was used for visualization
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3D visualization of connectivity between cortical and subcortical structures found to be different in people with hearing loss based on Tables and . Please refer to Figure for the possible roles these structures play in the auditory pathway. The lateral view of the left side of the gray/white surface of the JHU‐MNI‐SS template (Oishi et al., ) generated by FreeSurfer and transferred to native space (Fischl, ) is shown. The cortical structures (Pars Triangularis, Pars Opercularis, Superior Temporal Gyrus, Planum Temporale, Heschl's Gyrus), one subcortical structure (Thalamus), and the white matter Posterior Thalamic Radiation tract which contains the optic radiation were obtained from the JHU‐MNI‐SS labels and triangulated. The other white matter fasisculi structures were obtained from the IXI template (Yushkevich, Zhang, Simon, & Gee, ) and transferred via diffeomorphic mapping (Ceritoglu et al., ) of the IXI fractional anisotropy image to the corresponding JHU‐MNI‐SS image. Short range fiber tracts from the Heschl's Gyrus to Planum Temporale generated by dynamic programming (M. Li, Ratnanather, Miller, & Mori, ; Ratnanather et al., ) are partially hidden. CAWorks (www.cis.jhu.edu/software/caworks) was used for visualization
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Laboratory Methods and Technologies > Imaging
Translational, Genomic, and Systems Medicine > Translational Medicine
Developmental Biology > Developmental Processes in Health and Disease

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