Prefrontal cortex supports speech perception in listeners with cochlear implants

  1. Arefeh Sherafati
  2. Noel Dwyer
  3. Aahana Bajracharya
  4. Mahlega Samira Hassanpour
  5. Adam T Eggebrecht
  6. Jill B Firszt
  7. Joseph P Culver
  8. Jonathan Erik Peelle  Is a corresponding author
  1. Washington University in St. Louis, United States
  2. University of Utah, United States

Abstract

Cochlear implants are neuroprosthetic devices that can restore hearing in people with severe to profound hearing loss by electrically stimulating the auditory nerve. Because of physical limitations on the precision of this stimulation, the acoustic information delivered by a cochlear implant does not convey the same level of acoustic detail as that conveyed by normal hearing. As a result, speech understanding in listeners with cochlear implants is typically poorer and more effortful than in listeners with normal hearing. The brain networks supporting speech understanding in listeners with cochlear implants are not well understood, partly due to difficulties obtaining functional neuroimaging data in this population. In the current study, we assessed the brain regions supporting spoken word understanding in adult listeners with right unilateral cochlear implants (n=20) and matched controls (n=18) using high-density diffuse optical tomography (HD-DOT), a quiet and non-invasive imaging modality with spatial resolution comparable to that of functional MRI. We found that while listening to spoken words in quiet, listeners with cochlear implants showed greater activity in the left prefrontal cortex than listeners with normal hearing, specifically in a region engaged in a separate spatial working memory task. These results suggest that listeners with cochlear implants require greater cognitive processing during speech understanding than listeners with normal hearing, supported by compensatory recruitment of the left prefrontal cortex.

Data availability

Stimuli, data, and analysis scripts are available from https://osf.io/nkb5v/.

The following data sets were generated

Article and author information

Author details

  1. Arefeh Sherafati

    Department of Radiology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2543-0851
  2. Noel Dwyer

    Department of Otolaryngology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    No competing interests declared.
  3. Aahana Bajracharya

    Department of Otolaryngology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    No competing interests declared.
  4. Mahlega Samira Hassanpour

    moran Eye Center, University of Utah, Salt Lake City, United States
    Competing interests
    No competing interests declared.
  5. Adam T Eggebrecht

    Department of Radiology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    No competing interests declared.
  6. Jill B Firszt

    Department of Otolaryngology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    No competing interests declared.
  7. Joseph P Culver

    Department of Radiology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    No competing interests declared.
  8. Jonathan Erik Peelle

    Department of Otolaryngology, Washington University in St. Louis, Saint Louis, United States
    For correspondence
    jpeelle@wustl.edu
    Competing interests
    Jonathan Erik Peelle, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9194-854X

Funding

National Institutes of Health (R21DC015884)

  • Jonathan Erik Peelle

National Institutes of Health (R21DC016086)

  • Jonathan Erik Peelle

National Institutes of Health (K01MH103594)

  • Adam T Eggebrecht

National Institutes of Health (R21MH109775)

  • Adam T Eggebrecht

National Institutes of Health (R01NS090874)

  • Joseph P Culver

National Institutes of Health (R01NS109487)

  • Joseph P Culver

National Institutes of Health (R21DC015884)

  • Joseph P Culver

National Institutes of Health (R21DC016086)

  • Joseph P Culver

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

Ethics

Human subjects: All subjects were native speakers of English with no self-reported history of neurological or psychiatric disorders. All aspects of these studies were approved by the Human Research Protection Office (HRPO) of the Washington University School of Medicine. Subjects were recruited from the Washington University campus and the surrounding community (IRB 201101896, IRB 201709126). All subjects gave informed consent and were compensated for their participation in accordance with institutional and national guidelines.

Reviewing Editor

  1. Timothy D Griffiths, University of Newcastle, United Kingdom

Publication history

  1. Preprint posted: October 16, 2021 (view preprint)
  2. Received: November 5, 2021
  3. Accepted: June 4, 2022
  4. Accepted Manuscript published: June 6, 2022 (version 1)
  5. Version of Record published: June 23, 2022 (version 2)

Copyright

© 2022, Sherafati 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.

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  1. Arefeh Sherafati
  2. Noel Dwyer
  3. Aahana Bajracharya
  4. Mahlega Samira Hassanpour
  5. Adam T Eggebrecht
  6. Jill B Firszt
  7. Joseph P Culver
  8. Jonathan Erik Peelle
(2022)
Prefrontal cortex supports speech perception in listeners with cochlear implants
eLife 11:e75323.
https://doi.org/10.7554/eLife.75323

Further reading

    1. Developmental Biology
    2. Neuroscience
    Emily L Heckman, Chris Q Doe
    Research Advance

    The organization of neural circuits determines nervous system function. Variability can arise during neural circuit development (e.g. neurite morphology, axon/dendrite position). To ensure robust nervous system function, mechanisms must exist to accommodate variation in neurite positioning during circuit formation. Previously we developed a model system in the Drosophila ventral nerve cord to conditionally induce positional variability of a proprioceptive sensory axon terminal, and used this model to show that when we altered the presynaptic position of the sensory neuron, its major postsynaptic interneuron partner modified its dendritic arbor to match the presynaptic contact, resulting in functional synaptic input (Sales et al., 2019). Here we investigate the cellular mechanisms by which the interneuron dendrites detect and match variation in presynaptic partner location and input strength. We manipulate the presynaptic sensory neuron by (a) ablation; (b) silencing or activation; or (c) altering its location in the neuropil. From these experiments we conclude that there are two opposing mechanisms used to establish functional connectivity in the face of presynaptic variability: presynaptic contact stimulates dendrite outgrowth locally, whereas presynaptic activity inhibits postsynaptic dendrite outgrowth globally. These mechanisms are only active during an early larval critical period for structural plasticity. Collectively, our data provide new insights into dendrite development, identifying mechanisms that allow dendrites to flexibly respond to developmental variability in presynaptic location and input strength.

    1. Epidemiology and Global Health
    2. Neuroscience
    Lorenza Dall'Aglio, Hannah H Kim ... Henning Tiemeier
    Research Article Updated

    Background:

    Associations between attention-deficit/hyperactivity disorder (ADHD) and brain morphology have been reported, although with several inconsistencies. These may partly stem from confounding bias, which could distort associations and limit generalizability. We examined how associations between brain morphology and ADHD symptoms change with adjustments for potential confounders typically overlooked in the literature (aim 1), and for the intelligence quotient (IQ) and head motion, which are generally corrected for but play ambiguous roles (aim 2).

    Methods:

    Participants were 10-year-old children from the Adolescent Brain Cognitive Development (N = 7722) and Generation R (N = 2531) Studies. Cortical area, volume, and thickness were measured with MRI and ADHD symptoms with the Child Behavior Checklist. Surface-based cross-sectional analyses were run.

    Results:

    ADHD symptoms related to widespread cortical regions when solely adjusting for demographic factors. Additional adjustments for socioeconomic and maternal behavioral confounders (aim 1) generally attenuated associations, as cluster sizes halved and effect sizes substantially reduced. Cluster sizes further changed when including IQ and head motion (aim 2), however, we argue that adjustments might have introduced bias.

    Conclusions:

    Careful confounder selection and control can help identify more robust and specific regions of associations for ADHD symptoms, across two cohorts. We provided guidance to minimizing confounding bias in psychiatric neuroimaging.

    Funding:

    Authors are supported by an NWO-VICI grant (NWO-ZonMW: 016.VICI.170.200 to HT) for HT, LDA, SL, and the Sophia Foundation S18-20, and Erasmus University and Erasmus MC Fellowship for RLM.