Exposing distinct subcortical components of the auditory brainstem response evoked by continuous naturalistic speech

  1. Melissa J Polonenko
  2. Ross K Maddox  Is a corresponding author
  1. University of Rochester, United States

Abstract

Speech processing is built upon encoding by the auditory nerve and brainstem, yet we know very little about how these processes unfold in specific subcortical structures. These structures are deep and respond quickly, making them difficult to study during ongoing speech. Recent techniques begin to address this problem, but yield temporally broad responses with consequently ambiguous neural origins. Here we describe a method that pairs re-synthesized 'peaky' speech with deconvolution analysis of EEG recordings. We show that in adults with normal hearing, the method quickly yields robust responses whose component waves reflect activity from distinct subcortical structures spanning auditory nerve to rostral brainstem. We further demonstrate the versatility of peaky speech by simultaneously measuring bilateral and ear-specific responses across different frequency bands, and discuss important practical considerations such as talker choice. The peaky speech method holds promise as a tool for investigating speech encoding and processing, and for clinical applications.

Data availability

Python code is available on the lab GitHub account (https://github.com/maddoxlab/peaky-speech). All EEG recordings are posted in the EEG-BIDS format (Pernet et al., 2019) to Dryad (https://doi.org/10.5061/dryad.12jm63xwd). Stimulus files necessary to derive the peaky speech responses are deposited in the same Dryad repository.

The following data sets were generated

Article and author information

Author details

  1. Melissa J Polonenko

    Neuroscience, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1914-6117
  2. Ross K Maddox

    Neuroscience, Biomedical Engineering, University of Rochester, Rochester, United States
    For correspondence
    ross.maddox@rochester.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2668-0238

Funding

National Institute on Deafness and Other Communication Disorders (R00DC014288)

  • Ross K Maddox

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 gave written informed consent before the experiment began. All experimental procedures were approved by the University of Rochester Research Subjects Review Board. (#1227).

Copyright

© 2021, Polonenko & Maddox

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

  • 1,871
    views
  • 229
    downloads
  • 29
    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. Melissa J Polonenko
  2. Ross K Maddox
(2021)
Exposing distinct subcortical components of the auditory brainstem response evoked by continuous naturalistic speech
eLife 10:e62329.
https://doi.org/10.7554/eLife.62329

Share this article

https://doi.org/10.7554/eLife.62329

Further reading

    1. Developmental Biology
    2. Neuroscience
    Agnik Dasgupta, Caleb C Reagor ... AJ Hudspeth
    Research Article

    In a developing nervous system, axonal arbors often undergo complex rearrangements before neural circuits attain their final innervation topology. In the lateral line sensory system of the zebrafish, developing sensory axons reorganize their terminal arborization patterns to establish precise neural microcircuits around the mechanosensory hair cells. However, a quantitative understanding of the changes in the sensory arbor morphology and the regulators behind the microcircuit assembly remain enigmatic. Here, we report that Semaphorin7A (Sema7A) acts as an important mediator of these processes. Utilizing a semi-automated three-dimensional neurite tracing methodology and computational techniques, we have identified and quantitatively analyzed distinct topological features that shape the network in wild-type and Sema7A loss-of-function mutants. In contrast to those of wild-type animals, the sensory axons in Sema7A mutants display aberrant arborizations with disorganized network topology and diminished contacts to hair cells. Moreover, ectopic expression of a secreted form of Sema7A by non-hair cells induces chemotropic guidance of sensory axons. Our findings propose that Sema7A likely functions both as a juxtracrine and as a secreted cue to pattern neural circuitry during sensory organ development.

    1. Neuroscience
    Eun Joo Kim, Mi-Seon Kong ... Jeansok John Kim
    Research Article

    Pavlovian fear conditioning research suggests that the interaction between the dorsal periaqueductal gray (dPAG) and basolateral amygdala (BLA) acts as a prediction error mechanism in the formation of associative fear memories. However, their roles in responding to naturalistic predatory threats, characterized by less explicit cues and the absence of reiterative trial-and-error learning events, remain unexplored. In this study, we conducted single-unit recordings in rats during an ‘approach food-avoid predator’ task, focusing on the responsiveness of dPAG and BLA neurons to a rapidly approaching robot predator. Optogenetic stimulation of the dPAG triggered fleeing behaviors and increased BLA activity in naive rats. Notably, BLA neurons activated by dPAG stimulation displayed immediate responses to the robot, demonstrating heightened synchronous activity compared to BLA neurons that did not respond to dPAG stimulation. Additionally, the use of anterograde and retrograde tracer injections into the dPAG and BLA, respectively, coupled with c-Fos activation in response to predatory threats, indicates that the midline thalamus may play an intermediary role in innate antipredatory-defensive functioning.