Damage to the right insula disrupts the perception of affective touch

  1. Louise P Kirsch  Is a corresponding author
  2. Sahba Besharati
  3. Christina Papadaki
  4. Laura Crucianelli
  5. Sara Bertagnoli
  6. Nick Ward
  7. Valentina Moro
  8. Paul M Jenkinson
  9. Aikaterini Fotopoulou
  1. Sorbonne Universite, France
  2. University of the Witwatersrand, South Africa
  3. University College London, United Kingdom
  4. University of Verona, Italy
  5. University of Hertfordshire, United Kingdom

Abstract

Specific, peripheral C-tactile afferents contribute to the perception of tactile pleasure, but the brain areas involved in their processing remain debated. We report the first human lesion study on the perception of C-tactile touch in right hemisphere stroke patients (N = 59), revealing that right posterior and anterior insula lesions reduce tactile, contralateral and ipsilateral pleasantness sensitivity, respectively. These findings corroborate previous imaging studies regarding the role of the posterior insula in the perception of affective touch. However, our findings about the crucial role of the anterior insula for ipsilateral affective touch perception open new avenues of enquiry regarding the cortical organization of this tactile system.

Data availability

The data that support the findings of this study are available on the Open Science Framework (https://osf.io/fyrwc/?view_only=75773c749be84432994beca994481988).

The following data sets were generated

Article and author information

Author details

  1. Louise P Kirsch

    Institut des Systèmes Intelligents et de Robotique, Sorbonne Universite, Paris, France
    For correspondence
    kirsch.lou@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8418-776X
  2. Sahba Besharati

    The Department of Psychology, University of the Witwatersrand, Johannesburg, South Africa
    Competing interests
    The authors declare that no competing interests exist.
  3. Christina Papadaki

    Department of Clinical, Educational and Health Psychology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Laura Crucianelli

    Department of Clinical, Educational and Health Psychology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Sara Bertagnoli

    Department of Human Sciences, University of Verona, Verona, Italy
    Competing interests
    The authors declare that no competing interests exist.
  6. Nick Ward

    Sobell Department of Motor Neuroscience and Movement Disorders, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Valentina Moro

    Department of Human Sciences, University of Verona, Verona, Italy
    Competing interests
    The authors declare that no competing interests exist.
  8. Paul M Jenkinson

    Department of Psychology, School of Life and Medical Sciences, University of Hertfordshire, Hatfield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Aikaterini Fotopoulou

    Department of Clinical, Educational and Health Psychology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (ERC-2012-STG GA313755)

  • Aikaterini Fotopoulou

MIUR Italy (PRIN 20159CZFJK)

  • Valentina Moro

University of Verona (Bando di Ateneo per la Ricerca di Base 2015 project MOTOS)

  • Valentina Moro

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

Reviewing Editor

  1. Stephen Liberles, Harvard Medical School, United States

Ethics

Human subjects: All participants gave written, informed consent to take part in the study and to publish. The local National Health System Ethics Committees approved the study (REC:05/Q0706/218), which was carried out in accordance to the Declaration of Helsinki.

Version history

  1. Received: April 23, 2019
  2. Accepted: January 23, 2020
  3. Accepted Manuscript published: January 24, 2020 (version 1)
  4. Version of Record published: February 26, 2020 (version 2)

Copyright

© 2020, Kirsch 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

  • 3,805
    Page views
  • 351
    Downloads
  • 43
    Citations

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

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. Louise P Kirsch
  2. Sahba Besharati
  3. Christina Papadaki
  4. Laura Crucianelli
  5. Sara Bertagnoli
  6. Nick Ward
  7. Valentina Moro
  8. Paul M Jenkinson
  9. Aikaterini Fotopoulou
(2020)
Damage to the right insula disrupts the perception of affective touch
eLife 9:e47895.
https://doi.org/10.7554/eLife.47895

Share this article

https://doi.org/10.7554/eLife.47895

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.