1. Neuroscience
Download icon

Altered functional connectivity during speech perception in congenital amusia

  1. Kyle Jasmin  Is a corresponding author
  2. Frederic Dick
  3. Lauren Stewart
  4. Adam Taylor Tierney
  1. Birkbeck University of London, United Kingdom
  2. Goldsmiths University of London, United Kingdom
  3. Birkbeck, University of London, United Kingdom
Research Article
  • Cited 0
  • Views 414
  • Annotations
Cite this article as: eLife 2020;9:e53539 doi: 10.7554/eLife.53539

Abstract

Individuals with congenital amusia have a lifelong history of unreliable pitch processing. Accordingly, they downweight pitch cues during speech perception and instead rely on other dimensions such as duration. We investigated the neural basis for this strategy. During fMRI, individuals with amusia (N=15) and controls (N=15) read sentences where a comma indicated a grammatical phrase boundary. They then heard two sentences spoken that differed only in pitch and/or duration cues, and selected the best match for the written sentence. Prominent reductions in functional connectivity were detected in the amusia group, between left prefrontal language-related regions and right hemisphere pitch-related regions, which reflected the between-group differences in cue weights in the same groups of listeners. Connectivity differences between these regions were not present during a control task. Our results indicate that the reliability of perceptual dimensions is linked with functional connectivity between frontal and perceptual regions, and suggest a compensatory mechanism.

Article and author information

Author details

  1. Kyle Jasmin

    Psychological Sciences, Birkbeck University of London, London, United Kingdom
    For correspondence
    kyle.jasmin.11@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9723-8207
  2. Frederic Dick

    Psychological Sciences, Birkbeck University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2933-3912
  3. Lauren Stewart

    Psychology, Goldsmiths University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Adam Taylor Tierney

    Department of Psychological Sciences, Birkbeck, University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

Wellcome (109719/15/Z)

  • Adam Taylor Tierney

Leverhulme Trust (ECF-2017-151)

  • Kyle Jasmin

Society for Education, Music and Psychology Research

  • Kyle Jasmin

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 participants gave informed consent and ethical approval was obtained from the UCL Research Ethics Committee (fMRI/2016/001) and the Birkbeck Department of Psychology Research Ethics Committee (161711).

Reviewing Editor

  1. Andrew J Oxenham, University of Minnesota, United States

Publication history

  1. Received: November 12, 2019
  2. Accepted: August 3, 2020
  3. Accepted Manuscript published: August 7, 2020 (version 1)
  4. Version of Record published: August 26, 2020 (version 2)

Copyright

© 2020, Jasmin 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

  • 414
    Page views
  • 63
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Laura Gwilliams, Jean-Remi King
    Research Article Updated

    Perception depends on a complex interplay between feedforward and recurrent processing. Yet, while the former has been extensively characterized, the computational organization of the latter remains largely unknown. Here, we use magneto-encephalography to localize, track and decode the feedforward and recurrent processes of reading, as elicited by letters and digits whose level of ambiguity was parametrically manipulated. We first confirm that a feedforward response propagates through the ventral and dorsal pathways within the first 200 ms. The subsequent activity is distributed across temporal, parietal and prefrontal cortices, which sequentially generate five levels of representations culminating in action-specific motor signals. Our decoding analyses reveal that both the content and the timing of these brain responses are best explained by a hierarchy of recurrent neural assemblies, which both maintain and broadcast increasingly rich representations. Together, these results show how recurrent processes generate, over extended time periods, a cascade of decisions that ultimately accounts for subjects’ perceptual reports and reaction times.

    1. Neuroscience
    Vincent Huson et al.
    Research Advance Updated

    Previously, we showed that modulation of the energy barrier for synaptic vesicle fusion boosts release rates supralinearly (Schotten, 2015). Here we show that mouse hippocampal synapses employ this principle to trigger Ca2+-dependent vesicle release and post-tetanic potentiation (PTP). We assess energy barrier changes by fitting release kinetics in response to hypertonic sucrose. Mimicking activation of the C2A domain of the Ca2+-sensor Synaptotagmin-1 (Syt1), by adding a positive charge (Syt1D232N) or increasing its hydrophobicity (Syt14W), lowers the energy barrier. Removing Syt1 or impairing its release inhibitory function (Syt19Pro) increases spontaneous release without affecting the fusion barrier. Both phorbol esters and tetanic stimulation potentiate synaptic strength, and lower the energy barrier equally well in the presence and absence of Syt1. We propose a model where tetanic stimulation activates Syt1-independent mechanisms that lower the energy barrier and act additively with Syt1-dependent mechanisms to produce PTP by exerting multiplicative effects on release rates.