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Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations

While empathy to the pain of conspecific is evolutionary-ancient and is observed in rodents and in primates, it also integrates higher-order affective representations. Yet, it is unclear whether human empathy for pain is inborn or matures during development and what neural processes underpin its mat...

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Autores principales: Levy, Jonathan, Goldstein, Abraham, Pratt, Maayan, Feldman, Ruth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5788915/
https://www.ncbi.nlm.nih.gov/pubmed/29379042
http://dx.doi.org/10.1038/s41598-018-19810-3
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author Levy, Jonathan
Goldstein, Abraham
Pratt, Maayan
Feldman, Ruth
author_facet Levy, Jonathan
Goldstein, Abraham
Pratt, Maayan
Feldman, Ruth
author_sort Levy, Jonathan
collection PubMed
description While empathy to the pain of conspecific is evolutionary-ancient and is observed in rodents and in primates, it also integrates higher-order affective representations. Yet, it is unclear whether human empathy for pain is inborn or matures during development and what neural processes underpin its maturation. Using magnetoencephalography, we monitored the brain response of children, adolescents, and adults (n = 209) to others’ pain, testing the shift from childhood to adult functioning. Results indicate that children’s vicarious empathy for pain operates via rudimentary sensory predictions involving alpha oscillations in somatosensory cortex, while adults’ response recruits advanced mechanisms of updating sensory predictions and activating affective empathy in viceromotor cortex via higher-level representations involving beta- and gamma-band activity. Our findings suggest that full-blown empathy to others’ pain emerges only in adulthood and involves a shift from sensory self-based to interoceptive other-focused mechanisms that support human altruism, maintain self-other differentiation, modulate feedback to monitor other’s state, and activate a plan of action to alleviate other’s suffering.
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spelling pubmed-57889152018-02-08 Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations Levy, Jonathan Goldstein, Abraham Pratt, Maayan Feldman, Ruth Sci Rep Article While empathy to the pain of conspecific is evolutionary-ancient and is observed in rodents and in primates, it also integrates higher-order affective representations. Yet, it is unclear whether human empathy for pain is inborn or matures during development and what neural processes underpin its maturation. Using magnetoencephalography, we monitored the brain response of children, adolescents, and adults (n = 209) to others’ pain, testing the shift from childhood to adult functioning. Results indicate that children’s vicarious empathy for pain operates via rudimentary sensory predictions involving alpha oscillations in somatosensory cortex, while adults’ response recruits advanced mechanisms of updating sensory predictions and activating affective empathy in viceromotor cortex via higher-level representations involving beta- and gamma-band activity. Our findings suggest that full-blown empathy to others’ pain emerges only in adulthood and involves a shift from sensory self-based to interoceptive other-focused mechanisms that support human altruism, maintain self-other differentiation, modulate feedback to monitor other’s state, and activate a plan of action to alleviate other’s suffering. Nature Publishing Group UK 2018-01-29 /pmc/articles/PMC5788915/ /pubmed/29379042 http://dx.doi.org/10.1038/s41598-018-19810-3 Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Levy, Jonathan
Goldstein, Abraham
Pratt, Maayan
Feldman, Ruth
Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations
title Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations
title_full Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations
title_fullStr Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations
title_full_unstemmed Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations
title_short Maturation of Pain Empathy from Child to Adult Shifts from Single to Multiple Neural Rhythms to Support Interoceptive Representations
title_sort maturation of pain empathy from child to adult shifts from single to multiple neural rhythms to support interoceptive representations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5788915/
https://www.ncbi.nlm.nih.gov/pubmed/29379042
http://dx.doi.org/10.1038/s41598-018-19810-3
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