Impact of inner ear malformation and cochlear nerve deficiency on the development of auditory-language network in children with profound sensorineural hearing loss
- Department of Otolaryngology, Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, China
- Ear Institute, Shanghai Jiao Tong University School of Medicine, China
- Shanghai Key Laboratory of Translational Medicine on Ear and Nose diseases, China
- Department of Radiology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, China
- MR Collaboration, Siemens Healthineers Ltd, China
- MR Scientific Marketing, Siemens Healthineers Ltd, China
Figures
Figure 1
Segmentation of the subcortical auditory regions at group and individual levels.
Subcortical auditory regions are exhibited as red areas in the schematic diagrams and dotted lines in T1w images and st-DEC-TDI maps. All images are in the axial plane. Schematic diagrams for the CN, SOC, and IC were redrawn from Moore, 1987 and for the MGB from Duvernoys Atlas of the Human Brain Stem and Cerebellum (2009). Group-level segmentation was performed in the study-specific template averaged from all 10 normal-hearing controls. Images from one normal hearing control (male, 32 months old) and one profound SNHL patient (male, 32 months old) were selected to show individual-level segmentation. CN, cochlear nucleus; ICP, inferior cerebellar peduncle; PBB, ponto bulbar body; VSN, trigeminal spinal nucleus; VST, trigeminal spinal tract; IO, inferior olive; SOC, superior olivary complex; ML, medial lemniscus; MCP, medial cerebellar peduncle; IC, inferior colliculus; CIC, commissure of IC; LL, lateral lemniscus; PAG, periaqueductal grey; MGB, medial geniculate body; LGB, lateral geniculate body; SC, superior colliculus; RN, red nucleus; SN, substantia nigra; CST, corticospinal tract; St-DEC-TDI, short-tracks directionally encoded colour track density imaging; SNHL, sensorineural hearing loss.
Figure 2 with 2 supplements
In vivo tractography of the auditory pathway and the language pathway in the study-specific template.
(A, E) present schematic diagrams for the ascending auditory pathway and the language pathway, respectively. The auditory diagram was adapted from Duvernoys Atlas of the Human Brain Stem and Cerebellum (2009); the language diagram was adapted from Friederici et al., 2017. (B, F) show three-dimensional reconstructions of tractography results of the central auditory pathway and the language pathway, respectively, in the study-specific template (at group level averaged from all 10 normal-hearing controls). Fibre colours refer to the subdivisions in each pathway, corresponding with the schematic colours in (A) and (E). The ball-and-stick diagrams represent the relative region-of-interest (ROI) size and streamline numbers in each pathway. Tractography results are also displayed in the study-specific white matter fibre orientation distribution (FOD) template in (C) and (G), colour coded by subdivision, and in (D, H), colour coded by direction (red: left-right; green: anterior-posterior; blue: superior-inferior). See Figure 2—video 1 and Figure 2—video 2 for three-dimensional animated videos of these pathways.
Figure 2—video 1
Three-dimensional animated video of the central auditory pathway.
Figure 2—video 2
Three-dimensional animated video of the language pathway.
Figure 3 with 1 supplement
Fibre impairment of the central auditory pathway and the language pathway in children with profound sensorineural hearing loss (SNHL).
Streamlines associated with significantly reduced fibre cross-section (FC), fibre density (FD), and fibre density and cross-section (FDC) (family-wise error [FWE]-corrected p-value<0.05) in fixel-wise comparison between patients with profound SNHL (n=13) and normal hearing controls (n=10) are shown for the central auditory pathway (A) and the language pathway (B). The left two columns in each panel display colour coded by direction and the right two coded by absolute values of effect size. Mean FC, FD, and FDC extracted from pathway subdivisions, entire pathways, and impaired fixels from (A) and (B) in the central auditory pathway (C) and the language pathway (D) are shown for patients with profound SNHL versus normal hearing controls. ‘p’ represents the uncorrected p-value; ‘pFWE’ denotes the FWE-corrected p-value. Non-significant p-values, whether uncorrected or FWE-corrected, are not displayed in the figure. The error bars represent Standard Error of the Mean. Refer to Figure 3—figure supplement 1 for results displayed by separating three groups: profound SNHL with ear malformations and/or cochlear nerve deficiency (IEM&CND), profound SNHL with normal peripheral structure, and normal hearing controls.
Figure 3—figure supplement 1
Mean fibre cross-section (FC), fibre density (FD), and fibre density and cross-section (FDC) extracted from pathway subdivisions, entire pathways, and impaired fixels from Figure 3 (A) and Figure 3 (B) in the central auditory pathway and the language pathway of subjects from three groups: profound sensorineural hearing loss (SNHL) with ear malformations and/or cochlear nerve deficiency (IEM&CND) (n=6), profound SNHL with normal peripheral structure (n=7), and normal hearing controls (n=10).
The error bars represent Standard Error of the Mean.
Figure 4
Cranial nerve VIII median contrast values and central pathway fibre metrics in profound sensorineural hearing loss (SNHL) patients with normal peripheral structure (n=7) or those with ear malformations and/or cochlear nerve deficiency (IEM&CND) (n=5).
(A) shows temporal bone high-resolution CT (HRCT) and constructive interference in steady state (CISS) sections from a patient who underwent cochlear implantation (CI) surgery (male, 32 months old) and demonstrates a normal structure of the inner ear and cochlear nerve. (B) presents temporal bone HRCT and CISS sections from an auditory brainstem implantation (ABI) candidate (male, 17 months old) and reveals IEM&CND. The red arrow in (B) points to the missing cochlear nerve that is normally present, as shown by the red arrow in (A). (C) displays inverted CISS sections (axial plane) at the pontomedullary junction from a patient with profound SNHL. Cranial nerve VIII (cn.VIII) is visualized as a hyperintense structure relative to the surrounding cerebrospinal fluid (CSF). Cn.VIII was segmented (purple) and extracted for its median contrast value, regressing out surrounding CSF median values. (D) shows the cn.VIII median contrast values for patients with normal peripheral structure versus those with IEM&CND. (E) presents the mean fibre density (FD), fibre cross-section (FC), and fibre density and cross-section (FDC) of profound hearing loss-associated impaired fixels (from fixel-wise comparison results between patients and controls; see Figure 2A and B) in central pathways for patients with normal peripheral structure versus those with IEM&CND. (F) displays the Pearson correlation between cn.VIII median contrast values and the mean FD of entire central pathways for patients with profound SNHL. (G) illustrates the Pearson correlation between cn.VIII median contrast values and the mean FD of profound hearing loss-associated impaired fixels in central pathways for patients with profound SNHL. (H) demonstrates the moderation of central auditory pathway maturation by cn.VIII median contrast values. The mean FD of the entire central auditory pathway was significantly associated with age (beta value = 0.809), and their association was negatively moderated by cn.VIII median contrast values (interaction beta value = –0.379). (I) shows the moderation of language pathway maturation by cn.VIII median contrast values. The mean FD of the entire language pathway was significantly associated with age (beta value = 0.782), and their association was negatively moderated by cn.VIII median contrast values (interaction beta value = –0.298). These moderation effects are visualized as separate correlation plots of central pathway FD and age for patients with normal peripheral structure and those with IEM&CND. In panels (D–G), 'p’ represents the uncorrected p-value; ‘pFWE’ denotes the family-wise error (FWE)-corrected p-value. Non-significant p-values, whether uncorrected or FWE-corrected, are not displayed in the figure. The error bars represent Standard Error of the Mean. In panels (H) and (I), *p<0.05, **p<0.01, ***p<0.001. Refer to Figure 4—source data 2 for detailed statistics of the moderation analysis, as well as moderation analysis results after controlling gender, gestational weeks, and birth weights.
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Figure 4—source data 1
Pearson correlation between cn.VIII median contrast values and fibre metrics of central pathways.
- https://cdn.elifesciences.org/articles/85983/elife-85983-fig4-data1-v1.xlsx
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Figure 4—source data 2
Detailed statistics of moderation analyses.
(a) Moderation analysis of the effect of cn.VIII median contrast values on the relationship between auditory pathway fibre density (FD) and age. (b) Moderation analysis of the effect of cn.VIII median contrast values on the relationship between language pathway FD and age. (c) Moderation analysis of the effect of cn.VIII median contrast values on the relationship between auditory pathway FD and age, controlling gender, gestational weeks, and birth weights. (d) Moderation analysis of the effect of cn.VIII median contrast values on the relationship between language pathway FD and age, controlling gender, gestational weeks, and birth weights.
- https://cdn.elifesciences.org/articles/85983/elife-85983-fig4-data2-v1.xlsx
Figure 5 with 1 supplement
Correlations between preoperative characteristics and postoperative outcomes of auditory brainstem implantation (ABI) and cochlear implantation (CI) recipients.
The size of the bubble represents the correlation levels; the colour intensity of the bubble represents the uncorrected significance levels. All correlations deemed significant are positive. Start, at device activation; 6 m, at 6 mo post-activation; ∆6m, changes over the 6-month intervening period; PTA-6m, pure tone average at 6 mo post-activation; CAP, Categories of Auditory Performance; SIR, Speech Intelligibility of Rating; IT-MAIS, Infant-toddler Meaningful Auditory Integration Scale; MUSS, Meaningful Use of Speech Scale. For correlations specific to CI recipients, please refer to Figure 5—figure supplement 1.
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Figure 5—source data 1
Postoperative outcomes of auditory brainstem implantation (ABI) and cochlear implantation (CI) recipients.
- https://cdn.elifesciences.org/articles/85983/elife-85983-fig5-data1-v1.xlsx
Figure 5—figure supplement 1
Correlations between preoperative characteristics and postoperative outcomes of cochlear implantation (CI) recipients.
The size of the bubble represents the correlation levels; the colour intensity of the bubble represents the uncorrected significance levels. All correlations deemed significant are positive. Start, at device activation; 6m, at 6 mo post-activation; ∆6m, changes over the 6-month intervening period; PTA-6m, pure tone average at 6 mo post-activation; CAP, Categories of Auditory Performance; SIR, Speech Intelligibility of Rating; IT-MAIS, Infant-toddler Meaningful Auditory Integration Scale; MUSS, Meaningful Use of Speech Scale.
Figure 6
Comprehensive pre-surgical evaluation of the auditory-language network.
Tables
Table 1
Demographic information for patients with congenital bilateral profound sensorineural hearing loss.
| Gender | Age (mo) | Gestational weeks | Birth weight (kg) | Inner ear structure (CT) | Cochlear nerve (CISS) | Surgery |
|---|---|---|---|---|---|---|
| M | 26 | 39 | 3.25 | Cochlear aplasia | Deficiency | ABI |
| M | 24 | 39 | 2.7 | Normal | Normal | CI |
| F | 56 | 39 | 3.2 | Normal | Normal | CI |
| F | 65 | 39 | 2.9 | Normal | Normal | CI |
| M | 17 | 40 | 3.4 | Incomplete partition type I | Deficiency | ABI candidate |
| M | 32 | 40 | 3.3 | Normal | Normal | CI |
| M | 29 | 40 | 3 | Cochlear hypoplasia (L), Cochlear aplasia (R) | Deficiency | ABI |
| M | 14 | 40 | 2.9 | Normal | Normal | CI |
| M | 6 | 39 | 4.3 | Hypoplastic cochlear aperture | Deficiency | ABI candidate |
| F | 72 | 36 | 2.2 | Hypoplastic cochlear aperture | Deficiency | ABI candidate |
| M | 44 | 40 | 3.97 | Normal | Normal | CI |
| F | 9 | 40 | 3.6 | Normal | Normal | CI |
| M | 8 | 38 | 6 | Hypoplastic cochlear aperture | Deficiency | ABI candidate |
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ABI, auditory brainstem implantation; CI, cochlear implantation; CISS, constructive interference in steady state.
Additional files
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Supplementary file 1
Audiological characteristics of patients with congenital bilateral profound sensorineural hearing loss.
- https://cdn.elifesciences.org/articles/85983/elife-85983-supp1-v1.xlsx
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Supplementary file 2
Genetic profile of patients with congenital bilateral profound sensorineural hearing loss.
- https://cdn.elifesciences.org/articles/85983/elife-85983-supp2-v1.xlsx
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MDAR checklist
- https://cdn.elifesciences.org/articles/85983/elife-85983-mdarchecklist1-v1.docx
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Impact of inner ear malformation and cochlear nerve deficiency on the development of auditory-language network in children with profound sensorineural hearing loss
eLife 12:e85983.
https://doi.org/10.7554/eLife.85983
