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Neural preservation underlies speech improvement from auditory deprivation in young cochlear implant recipients

Gangyi Feng, Erin M. Ingvalson, Tina M. Grieco-Calub, Megan Y. Roberts, Maura E. Ryan, Patrick Birmingham, Delilah Burrowes, Nancy M. Young, and Patrick C. M. Wong
PNAS January 30, 2018 115 (5) E1022-E1031; published ahead of print January 16, 2018 https://doi.org/10.1073/pnas.1717603115
Gangyi Feng
aDepartment of Linguistics and Modern Languages, The Chinese University of Hong Kong, Hong Kong SAR, China;bBrain and Mind Institute, The Chinese University of Hong Kong, Hong Kong SAR, China;
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Erin M. Ingvalson
cSchool of Communication Science and Disorders, Florida State University, Tallahassee, FL 32301;dDepartment of Otolaryngology - Head and Neck Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;
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  • ORCID record for Erin M. Ingvalson
Tina M. Grieco-Calub
eRoxelyn and Richard Pepper Department of Communication Sciences and Disorders, Northwestern University, Evanston, IL 60208;fKnowles Hearing Center, School of Communication, Northwestern University, Evanston, IL 60208;
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Megan Y. Roberts
eRoxelyn and Richard Pepper Department of Communication Sciences and Disorders, Northwestern University, Evanston, IL 60208;
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Maura E. Ryan
gDepartment of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;hDepartment of Medical Imaging, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL 60611;
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Patrick Birmingham
iDepartment of Anesthesiology, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL 60611;jDepartment of Anesthesiology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;
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Delilah Burrowes
gDepartment of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;hDepartment of Medical Imaging, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL 60611;
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Nancy M. Young
dDepartment of Otolaryngology - Head and Neck Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;fKnowles Hearing Center, School of Communication, Northwestern University, Evanston, IL 60208;kDivision of Otolaryngology - Head and Neck Surgery, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL 60611;
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Patrick C. M. Wong
aDepartment of Linguistics and Modern Languages, The Chinese University of Hong Kong, Hong Kong SAR, China;bBrain and Mind Institute, The Chinese University of Hong Kong, Hong Kong SAR, China;lDepartment of Otorhinolaryngology, Head and Neck Surgery, The Chinese University of Hong Kong, Hong Kong SAR, China
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  • For correspondence: p.wong@cuhk.edu.hk
  1. Edited by Robert J. Zatorre, Montreal Neurological Institute, McGill University, Montreal, QC, Canada, and accepted by Editorial Board Member Thomas D. Albright December 6, 2017 (received for review October 17, 2017)

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Significance

The ability to accurately predict speech improvement for young children who use cochlear implants (CIs) would be a first step in the development of a personalized therapy to enhance language development. Despite decades of outcome research, no useful clinical prediction tool exists. An accurate predictive model that relies on routinely obtained presurgical neuroanatomic data has the potential to transform clinical practice while enhancing our understanding of neural organization resulting from auditory deprivation. Using presurgical MRI neuroanatomical data and multivariate pattern analysis techniques, we found that neural systems that were unaffected by auditory deprivation best predicted young CI candidates’ postsurgical speech-perception outcomes. Our study provides an example of how research in cognitive neuroscience can inform basic science and lead to clinical application.

Abstract

Although cochlear implantation enables some children to attain age-appropriate speech and language development, communicative delays persist in others, and outcomes are quite variable and difficult to predict, even for children implanted early in life. To understand the neurobiological basis of this variability, we used presurgical neural morphological data obtained from MRI of individual pediatric cochlear implant (CI) candidates implanted younger than 3.5 years to predict variability of their speech-perception improvement after surgery. We first compared neuroanatomical density and spatial pattern similarity of CI candidates to that of age-matched children with normal hearing, which allowed us to detail neuroanatomical networks that were either affected or unaffected by auditory deprivation. This information enables us to build machine-learning models to predict the individual children’s speech development following CI. We found that regions of the brain that were unaffected by auditory deprivation, in particular the auditory association and cognitive brain regions, produced the highest accuracy, specificity, and sensitivity in patient classification and the most precise prediction results. These findings suggest that brain areas unaffected by auditory deprivation are critical to developing closer to typical speech outcomes. Moreover, the findings suggest that determination of the type of neural reorganization caused by auditory deprivation before implantation is valuable for predicting post-CI language outcomes for young children.

  • neural preservation
  • cochlear implant
  • prediction
  • auditory deprivation
  • machine learning

Footnotes

  • ↵1To whom correspondence should be addressed. Email: p.wong{at}cuhk.edu.hk.
  • Author contributions: G.F., E.M.I., N.M.Y., and P.C.M.W. designed research; E.M.I., T.M.G.-C., M.Y.R., M.E.R., P.B., D.B., and N.M.Y. performed research; G.F. and E.M.I. analyzed data; and G.F., N.M.Y. and P.C.M.W. wrote the paper.

  • Conflict of interest statement: G.F., N.M.Y., P.C.M.W., The Chinese University of Hong Kong, and the Ann & Robert H. Lurie Children's Hospital of Chicago disclose potential financial conflict of interest related to US patent application filed on December 21, 2017.

  • This article is a PNAS Direct Submission. R.J.Z. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1717603115/-/DCSupplemental.

Published under the PNAS license.

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Neural preservation predicts speech outcomes in CI
Gangyi Feng, Erin M. Ingvalson, Tina M. Grieco-Calub, Megan Y. Roberts, Maura E. Ryan, Patrick Birmingham, Delilah Burrowes, Nancy M. Young, Patrick C. M. Wong
Proceedings of the National Academy of Sciences Jan 2018, 115 (5) E1022-E1031; DOI: 10.1073/pnas.1717603115

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Neural preservation predicts speech outcomes in CI
Gangyi Feng, Erin M. Ingvalson, Tina M. Grieco-Calub, Megan Y. Roberts, Maura E. Ryan, Patrick Birmingham, Delilah Burrowes, Nancy M. Young, Patrick C. M. Wong
Proceedings of the National Academy of Sciences Jan 2018, 115 (5) E1022-E1031; DOI: 10.1073/pnas.1717603115
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