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.

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.

Metrics

  • 1,800
    views
  • 367
    downloads
  • 18
    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. 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

Share this article

https://doi.org/10.7554/eLife.75323

Further reading

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience
    Gáspár Oláh, Rajmund Lákovics ... Gábor Tamás
    Research Article

    Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.