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Distinction of self-produced touch and social touch at cortical and spinal cord levels
Differentiation between self-produced tactile stimuli and touch by others is necessary for social interactions and for a coherent concept of “self.” The mechanisms underlying this distinction are unknown. Here, we investigated the distinction between self- and other-produced light touch in healthy v...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6369791/ https://www.ncbi.nlm.nih.gov/pubmed/30670645 http://dx.doi.org/10.1073/pnas.1816278116 |
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author | Boehme, Rebecca Hauser, Steven Gerling, Gregory J. Heilig, Markus Olausson, Håkan |
author_facet | Boehme, Rebecca Hauser, Steven Gerling, Gregory J. Heilig, Markus Olausson, Håkan |
author_sort | Boehme, Rebecca |
collection | PubMed |
description | Differentiation between self-produced tactile stimuli and touch by others is necessary for social interactions and for a coherent concept of “self.” The mechanisms underlying this distinction are unknown. Here, we investigated the distinction between self- and other-produced light touch in healthy volunteers using three different approaches: fMRI, behavioral testing, and somatosensory-evoked potentials (SEPs) at spinal and cortical levels. Using fMRI, we found self–other differentiation in somatosensory and sociocognitive areas. Other-touch was related to activation in several areas, including somatosensory cortex, insula, superior temporal gyrus, supramarginal gyrus, striatum, amygdala, cerebellum, and prefrontal cortex. During self-touch, we instead found deactivation in insula, anterior cingulate cortex, superior temporal gyrus, amygdala, parahippocampal gyrus, and prefrontal areas. Deactivation extended into brain areas encoding low-level sensory representations, including thalamus and brainstem. These findings were replicated in a second cohort. During self-touch, the sensorimotor cortex was functionally connected to the insula, and the threshold for detection of an additional tactile stimulus was elevated. Differential encoding of self- vs. other-touch during fMRI correlated with the individual self-concept strength. In SEP, cortical amplitudes were reduced during self-touch, while latencies at cortical and spinal levels were faster for other-touch. We thus demonstrated a robust self–other distinction in brain areas related to somatosensory, social cognitive, and interoceptive processing. Signs of this distinction were evident at the spinal cord. Our results provide a framework for future studies in autism, schizophrenia, and emotionally unstable personality disorder, conditions where symptoms include social touch avoidance and poor self-vs.-other discrimination. |
format | Online Article Text |
id | pubmed-6369791 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-63697912019-02-14 Distinction of self-produced touch and social touch at cortical and spinal cord levels Boehme, Rebecca Hauser, Steven Gerling, Gregory J. Heilig, Markus Olausson, Håkan Proc Natl Acad Sci U S A PNAS Plus Differentiation between self-produced tactile stimuli and touch by others is necessary for social interactions and for a coherent concept of “self.” The mechanisms underlying this distinction are unknown. Here, we investigated the distinction between self- and other-produced light touch in healthy volunteers using three different approaches: fMRI, behavioral testing, and somatosensory-evoked potentials (SEPs) at spinal and cortical levels. Using fMRI, we found self–other differentiation in somatosensory and sociocognitive areas. Other-touch was related to activation in several areas, including somatosensory cortex, insula, superior temporal gyrus, supramarginal gyrus, striatum, amygdala, cerebellum, and prefrontal cortex. During self-touch, we instead found deactivation in insula, anterior cingulate cortex, superior temporal gyrus, amygdala, parahippocampal gyrus, and prefrontal areas. Deactivation extended into brain areas encoding low-level sensory representations, including thalamus and brainstem. These findings were replicated in a second cohort. During self-touch, the sensorimotor cortex was functionally connected to the insula, and the threshold for detection of an additional tactile stimulus was elevated. Differential encoding of self- vs. other-touch during fMRI correlated with the individual self-concept strength. In SEP, cortical amplitudes were reduced during self-touch, while latencies at cortical and spinal levels were faster for other-touch. We thus demonstrated a robust self–other distinction in brain areas related to somatosensory, social cognitive, and interoceptive processing. Signs of this distinction were evident at the spinal cord. Our results provide a framework for future studies in autism, schizophrenia, and emotionally unstable personality disorder, conditions where symptoms include social touch avoidance and poor self-vs.-other discrimination. National Academy of Sciences 2019-02-05 2019-01-22 /pmc/articles/PMC6369791/ /pubmed/30670645 http://dx.doi.org/10.1073/pnas.1816278116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | PNAS Plus Boehme, Rebecca Hauser, Steven Gerling, Gregory J. Heilig, Markus Olausson, Håkan Distinction of self-produced touch and social touch at cortical and spinal cord levels |
title | Distinction of self-produced touch and social touch at cortical and spinal cord levels |
title_full | Distinction of self-produced touch and social touch at cortical and spinal cord levels |
title_fullStr | Distinction of self-produced touch and social touch at cortical and spinal cord levels |
title_full_unstemmed | Distinction of self-produced touch and social touch at cortical and spinal cord levels |
title_short | Distinction of self-produced touch and social touch at cortical and spinal cord levels |
title_sort | distinction of self-produced touch and social touch at cortical and spinal cord levels |
topic | PNAS Plus |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6369791/ https://www.ncbi.nlm.nih.gov/pubmed/30670645 http://dx.doi.org/10.1073/pnas.1816278116 |
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