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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...

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Autores principales: Boehme, Rebecca, Hauser, Steven, Gerling, Gregory J., Heilig, Markus, Olausson, Håkan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
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.
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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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