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.

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.

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

  • 4,109
    views
  • 380
    downloads
  • 61
    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. 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
    Ning Wang, Yimeng Wang ... Dong Ming
    Research Article

    The experience-dependent spatial cognitive process requires sequential organization of hippocampal neural activities by theta rhythm, which develops to represent highly compressed information for rapid learning. However, how the theta sequences were developed in a finer timescale within theta cycles remains unclear. In this study, we found in rats that sweep-ahead structure of theta sequences developing with exploration was predominantly dependent on a relatively large proportion of FG-cells, that is a subset of place cells dominantly phase-locked to fast gamma rhythms. These ensembles integrated compressed spatial information by cells consistently firing at precessing slow gamma phases within the theta cycle. Accordingly, the sweep-ahead structure of FG-cell sequences was positively correlated with the intensity of slow gamma phase precession, in particular during early development of theta sequences. These findings highlight the dynamic network modulation by fast and slow gamma in the development of theta sequences which may further facilitate memory encoding and retrieval.

    1. Neuroscience
    Muad Y Abd El Hay, Gretel B Kamm ... Jan Siemens
    Research Article

    The perception of innocuous temperatures is crucial for thermoregulation. The TRP ion channels TRPV1 and TRPM2 have been implicated in warmth detection, yet their precise roles remain unclear. A key challenge is the low prevalence of warmth-sensitive sensory neurons, comprising fewer than 10% of rodent dorsal root ganglion (DRG) neurons. Using calcium imaging of >20,000 cultured mouse DRG neurons, we uncovered distinct contributions of TRPV1 and TRPM2 to warmth sensitivity. TRPV1’s absence – and to a lesser extent absence of TRPM2 – reduces the number of neurons responding to warmth. Additionally, TRPV1 mediates the rapid, dynamic response to a warmth challenge. Behavioural tracking in a whole-body thermal preference assay revealed that these cellular differences shape nuanced thermal behaviours. Drift diffusion modelling of decision-making in mice exposed to varying temperatures showed that TRPV1 deletion impairs evidence accumulation, reducing the precision of thermal choice, while TRPM2 deletion increases overall preference for warmer environments that wildtype mice avoid. It remains unclear whether TRPM2 in DRG sensory neurons or elsewhere mediates thermal preference. Our findings suggest that different aspects of thermal information, such as stimulation speed and temperature magnitude, are encoded by distinct TRP channel mechanisms.