Functional brain alterations following mild-to-moderate sensorineural hearing loss in children

  1. Axelle Calcus  Is a corresponding author
  2. Outi Tuomainen
  3. Ana Campos
  4. Stuart Rosen
  5. Lorna F Halliday
  1. Ecole Normale Supérieure, France
  2. University College London, United Kingdom

Abstract

Auditory deprivation in the form of deafness during development leads to lasting changes in central auditory system function. However, less is known about the effects of mild-to-moderate sensorineural hearing loss (MMHL) during development. Here, we used a longitudinal design to examine late auditory evoked responses and mismatch responses to nonspeech and speech sounds for children with MMHL. At Time 1, younger children with MMHL (8-12 years; n = 23) showed age-appropriate mismatch negativities (MMNs) to sounds, but older children (12-16 years; n = 23) did not. Six years later, we re-tested a subset of the younger (now older) children with MMHL (n = 13). Children who had shown significant MMNs at Time 1 showed MMNs that were reduced and, for nonspeech, absent at Time 2. Our findings demonstrate that even a mild-to-moderate hearing loss during early-to-mid childhood can lead to changes in the neural processing of sounds in late childhood/adolescence.

Data availability

Unidentifiable data, stimuli, and statistical analyses scripts are available on https://github.com/acalcus/MMHL.git

The following data sets were generated

Article and author information

Author details

  1. Axelle Calcus

    Département d'Etudes Cognitives, Ecole Normale Supérieure, Paris, France
    For correspondence
    axelle.calcus@ens.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1240-1122
  2. Outi Tuomainen

    Department of Speech, Hearing and Phonetic Sciences, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Ana Campos

    Department of Speech, Hearing and Phonetic Sciences, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Stuart Rosen

    Department of Speech, Hearing and Phonetic Sciences, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Lorna F Halliday

    Department of Speech, Hearing and Phonetic Sciences, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

H2020 Marie Skłodowska-Curie Actions (FP7-607139)

  • Axelle Calcus

ESRC National Centre for Research Methods, University of Southampton (RES-061-25-0440)

  • Lorna F Halliday

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jonathan Erik Peelle, Washington University in St. Louis, United States

Ethics

Human subjects: Informed consent, and consent to publish was obtained from parents/guardians of the children included in this study. Ethical approval for this study was provided by the UCL Research Ethics Committee (Project ID number: 2109/004).

Version history

  1. Received: March 18, 2019
  2. Accepted: September 7, 2019
  3. Accepted Manuscript published: October 1, 2019 (version 1)
  4. Version of Record published: November 4, 2019 (version 2)

Copyright

© 2019, Calcus et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,777
    views
  • 424
    downloads
  • 13
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Axelle Calcus
  2. Outi Tuomainen
  3. Ana Campos
  4. Stuart Rosen
  5. Lorna F Halliday
(2019)
Functional brain alterations following mild-to-moderate sensorineural hearing loss in children
eLife 8:e46965.
https://doi.org/10.7554/eLife.46965

Share this article

https://doi.org/10.7554/eLife.46965

Further reading

    1. Neuroscience
    Alina Tetereva, Narun Pat
    Research Article

    One well-known biomarker candidate that supposedly helps capture fluid cognition is Brain Age, or a predicted value based on machine-learning models built to predict chronological age from brain MRI. To formally evaluate the utility of Brain Age for capturing fluid cognition, we built 26 age-prediction models for Brain Age based on different combinations of MRI modalities, using the Human Connectome Project in Aging (n=504, 36–100 years old). First, based on commonality analyses, we found a large overlap between Brain Age and chronological age: Brain Age could uniquely add only around 1.6% in explaining variation in fluid cognition over and above chronological age. Second, the age-prediction models that performed better at predicting chronological age did NOT necessarily create better Brain Age for capturing fluid cognition over and above chronological age. Instead, better-performing age-prediction models created Brain Age that overlapped larger with chronological age, up to around 29% out of 32%, in explaining fluid cognition. Third, Brain Age missed around 11% of the total variation in fluid cognition that could have been explained by the brain variation. That is, directly predicting fluid cognition from brain MRI data (instead of relying on Brain Age and chronological age) could lead to around a 1/3-time improvement of the total variation explained. Accordingly, we demonstrated the limited utility of Brain Age as a biomarker for fluid cognition and made some suggestions to ensure the utility of Brain Age in explaining fluid cognition and other phenotypes of interest.

    1. Developmental Biology
    2. Neuroscience
    Jonathan AC Menzies, André Maia Chagas ... Claudio R Alonso
    Research Article

    Movement is a key feature of animal systems, yet its embryonic origins are not fully understood. Here, we investigate the genetic basis underlying the embryonic onset of movement in Drosophila focusing on the role played by small non-coding RNAs (microRNAs, miRNAs). To this end, we first develop a quantitative behavioural pipeline capable of tracking embryonic movement in large populations of fly embryos, and using this system, discover that the Drosophila miRNA miR-2b-1 plays a role in the emergence of movement. Through the combination of spectral analysis of embryonic motor patterns, cell sorting and RNA in situs, genetic reconstitution tests, and neural optical imaging we define that miR-2b-1 influences the emergence of embryonic movement by exerting actions in the developing nervous system. Furthermore, through the combination of bioinformatics coupled to genetic manipulation of miRNA expression and phenocopy tests we identify a previously uncharacterised (but evolutionarily conserved) chloride channel encoding gene – which we term Movement Modulator (Motor) – as a genetic target that mechanistically links miR-2b-1 to the onset of movement. Cell-specific genetic reconstitution of miR-2b-1 expression in a null miRNA mutant background, followed by behavioural assays and target gene analyses, suggest that miR-2b-1 affects the emergence of movement through effects in sensory elements of the embryonic circuitry, rather than in the motor domain. Our work thus reports the first miRNA system capable of regulating embryonic movement, suggesting that other miRNAs are likely to play a role in this key developmental process in Drosophila as well as in other species.