Impact of inner ear malformation and cochlear nerve deficiency on the development of auditory-language network in children with profound sensorineural hearing loss

  1. Yaoxuan Wang
  2. Mengda Jiang
  3. Yuting Zhu
  4. Lu Xue
  5. Wenying Shu
  6. Xiang Li
  7. Hongsai Chen
  8. Yun Li
  9. Ying Chen
  10. Yongchuan Chai
  11. Yu Zhang
  12. Yinghua Chu
  13. Yang Song
  14. Xiaofeng Tao
  15. Zhaoyan Wang
  16. Hao Wu

  • Curated by eLife

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    This important study used high-resolution brain imaging methods to visualize and index non-invasively auditory and language pathways of young children born with inner ear malformations or cochlear nerve dysfunction resulting in profound hearing loss. Nerve fiber impairments were compellingly demonstrated in subcortical auditory and cortical language pathways relative to typically-hearing controls. The results suggested novel approaches for clinical assessment of central auditory and language pathways that may influence different intervention strategies, pending further evidence linking these structural findings with functional outcomes.

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Abstract

Profound congenital sensorineural hearing loss (SNHL) prevents children from developing spoken language. Cochlear implantation and auditory brainstem implantation can provide partial hearing sensation, but language development outcomes can vary, particularly for patients with inner ear malformations and/or cochlear nerve deficiency (IEM&CND). Currently, the peripheral auditory structure is evaluated through visual inspection of clinical imaging, but this method is insufficient for surgical planning and prognosis. The central auditory pathway is also challenging to examine in vivo due to its delicate subcortical structures. Previous attempts to locate subcortical auditory nuclei using fMRI responses to sounds are not applicable to patients with profound hearing loss as no auditory brainstem responses can be detected in these individuals, making it impossible to capture corresponding blood oxygen signals in fMRI. In this study, we developed a new pipeline for mapping the auditory pathway using structural and diffusional MRI. We used a fixel-based approach to investigate the structural development of the auditory-language network for profound SNHL children with normal peripheral structure and those with IEM&CND under 6 years old. Our findings indicate that the language pathway is more sensitive to peripheral auditory condition than the central auditory pathway, highlighting the importance of early intervention for profound SNHL children to provide timely speech inputs. We also propose a comprehensive pre-surgical evaluation extending from the cochlea to the auditory-language network, showing significant correlations between age, gender, Cn.VIII median contrast value, and the language network with post-implant qualitative outcomes.

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  1. Version published to 10.7554/elife.85983 on eLife
  2. eLife

    eLife assessment

    This important study used high-resolution brain imaging methods to visualize and index non-invasively auditory and language pathways of young children born with inner ear malformations or cochlear nerve dysfunction resulting in profound hearing loss. Nerve fiber impairments were compellingly demonstrated in subcortical auditory and cortical language pathways relative to typically-hearing controls. The results suggested novel approaches for clinical assessment of central auditory and language pathways that may influence different intervention strategies, pending further evidence linking these structural findings with functional outcomes.

  3. eLife

    Reviewer #1 (Public Review):

    In this study, Wang et al performed structural peripheral and central imaging of the auditory pathway using high-resolution MR. For the first time, they evaluated children with congenital severe to profound sensorineural hearing loss with and without cochlear nerve deficiency and cochlear malformations. The authors evaluated 13 children with severe to profound congenital hearing loss (6 with cochlear nerve deficiency) and 10 typically-hearing controls. They found significant differences in the central auditory pathway that were influenced by the status of the peripheral auditory pathway. Determination of outcomes after cochlear implantation or auditory brainstem implantation is critical and we currently have no good methods for this, so this study is very promising in that regard.

    The authors have achieved their aim of evaluating these children with high-resolution imaging and identifying differences in auditory pathways. My primary issues are that some of their claims for clinical potential are not justified as of yet and the authors did not determine a diagnosis for the patients' hearing loss.

  4. eLife

    Reviewer #2 (Public Review):

    The aim of this work is to introduce a new pipeline for mapping the human auditory pathway using structural and diffusional MRI, and to examine the brain structural development of children with profound congenital sensorineural hearing loss (SNHL) at both the acoustic processing level and the speech perception level. The authors use this pipeline to investigate the structural development of the auditory-language network for profound SNHL children with normal peripheral structure and those with inner ear malformations and/or cochlear nerve deficiency (IEM&CND). The authors successfully developed a new pipeline for reconstructing the human auditory pathway and used it to investigate the structural development of the auditory-language network in children with profound SNHL. They segmented the subcortical auditory nuclei using super-resolution track density imaging (TDI) maps and T1-weighted images and tracked the auditory and language pathways using probabilistic tractography. The authors found that the language pathway was more sensitive to peripheral auditory condition than the central auditory pathway, highlighting the importance of early intervention for profound SNHL children to provide timely speech inputs. The authors also proposed a comprehensive pre-surgical evaluation extending from the cochlea to the auditory-language network, which has promising clinical potential.

    The major strengths of this work are the use of a new pipeline for mapping the human auditory pathway, the inclusion of children with profound SNHL with and without IEM&CND, and the finding that the language pathway is more sensitive to peripheral auditory condition than the central auditory pathway. However, a limitation of this study is the small sample size, which may limit the generalizability of the findings.

    The results support the conclusions that the language pathway is more sensitive to peripheral auditory condition than the central auditory pathway, highlighting the importance of early intervention for profound SNHL children to provide timely speech inputs.

    This work has the potential to have a significant impact on the field by providing new insights into the structural development of the auditory-language network in children with profound SNHL. The methods and data presented in this work may be useful to the community in developing comprehensive pre-surgical evaluation for children with profound SNHL extending from the cochlea to the auditory-language network.

  5. eLife

    Reviewer #3 (Public Review):

    This study presents a new pipeline for mapping the auditory-language pathway in children with profound congenital sensorineural hearing loss (SNHL), focusing on those with inner ear malformations and/or cochlear nerve deficiency (IEM&CND). Using structural and diffusional MRI, the researchers investigated the structural fiber properties of the auditory-language networks in affected children under six years old. Findings suggest that the language pathway is more sensitive to peripheral auditory than the central auditory pathway, emphasizing the need for early intervention to provide speech inputs. The study also proposes a comprehensive pre-surgical evaluation from the cochlea to the auditory-language network.

    Strengths:

    1. Investigating fiber properties across various brain network levels (from peripheral structures to central auditory and higher-level language pathways) using high-resolution diffusion imaging and an innovative pipeline.

    2. Evaluating presurgical fiber properties in two subgroups of SNHL children (cochlear implant and auditory brainstem implant candidates) to demonstrate the relationship between peripheral auditory structure damage and the development of auditory-language structural pathways.

    Weaknesses:

    1. Limited sample size: The study analyzed data from 13 SNHL children and 10 normal-hearing children, potentially restricting the validity and reproducibility of the findings, particularly in correlation results based on individual differences.

    2. Lack of speech and language behavioral measures: Although the researchers collected behavioral data post-CI/ABI surgery for most participants, no such data was reported. Consequently, the association between presurgical fiber measures and postsurgical outcomes remains unclear.

    3. Unclear practical implications: The relevance of the presurgical evaluation of the auditory-language network for surgical decision-making and prognosis estimation is not evident, as fiber measures may not correlate with behavioral outcomes.

  6. Version published to 10.1101/2023.02.09.527841v1 on bioRxiv