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

  • 1,785
    views
  • 365
    downloads
  • 17
    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
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.

    1. Neuroscience
    Ulrike Pech, Jasper Janssens ... Patrik Verstreken
    Research Article

    The classical diagnosis of Parkinsonism is based on motor symptoms that are the consequence of nigrostriatal pathway dysfunction and reduced dopaminergic output. However, a decade prior to the emergence of motor issues, patients frequently experience non-motor symptoms, such as a reduced sense of smell (hyposmia). The cellular and molecular bases for these early defects remain enigmatic. To explore this, we developed a new collection of five fruit fly models of familial Parkinsonism and conducted single-cell RNA sequencing on young brains of these models. Interestingly, cholinergic projection neurons are the most vulnerable cells, and genes associated with presynaptic function are the most deregulated. Additional single nucleus sequencing of three specific brain regions of Parkinson’s disease patients confirms these findings. Indeed, the disturbances lead to early synaptic dysfunction, notably affecting cholinergic olfactory projection neurons crucial for olfactory function in flies. Correcting these defects specifically in olfactory cholinergic interneurons in flies or inducing cholinergic signaling in Parkinson mutant human induced dopaminergic neurons in vitro using nicotine, both rescue age-dependent dopaminergic neuron decline. Hence, our research uncovers that one of the earliest indicators of disease in five different models of familial Parkinsonism is synaptic dysfunction in higher-order cholinergic projection neurons and this contributes to the development of hyposmia. Furthermore, the shared pathways of synaptic failure in these cholinergic neurons ultimately contribute to dopaminergic dysfunction later in life.