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Words hurt: common and distinct neural substrates underlying nociceptive and semantic pain

Frontiers in neuroscience, 2023-09, Vol.17, p.1234286-1234286 [Peer Reviewed Journal]

2023. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. ;Copyright © 2023 Borelli, Benuzzi, Ballotta, Bandieri, Luppi, Cacciari, Porro and Lui. 2023 Borelli, Benuzzi, Ballotta, Bandieri, Luppi, Cacciari, Porro and Lui ;ISSN: 1662-453X ;ISSN: 1662-4548 ;EISSN: 1662-453X ;DOI: 10.3389/fnins.2023.1234286

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  • Title:
    Words hurt: common and distinct neural substrates underlying nociceptive and semantic pain
  • Author: Borelli, Eleonora ; Benuzzi, Francesca ; Ballotta, Daniela ; Bandieri, Elena ; Luppi, Mario ; Cacciari, Cristina ; Porro, Carlo Adolfo ; Lui, Fausta
  • Subjects: Arousal ; Brain ; Brain mapping ; Cortex (cingulate) ; Females ; Functional magnetic resonance imaging ; Information processing ; language ; Medical imaging ; Neuroimaging ; Neuroscience ; Pain ; Pain perception ; physical pain-related words ; Prefrontal cortex ; Semantics ; Social exclusion ; social pain-related words ; Thalamus ; words
  • Is Part Of: Frontiers in neuroscience, 2023-09, Vol.17, p.1234286-1234286
  • Description: Introduction Recent studies have shown that processing semantic pain, such as words associated with physical pain, modulates pain perception and enhances activity in regions of the pain matrix. A direct comparison between activations due to noxious stimulation and processing of words conveying physical pain may clarify whether and to what extent the neural substrates of nociceptive pain are shared by semantic pain. Pain is triggered also by experiences of social exclusion, rejection or loss of significant others (the so-called social pain), therefore words expressing social pain may modulate pain perception similarly to what happens with words associated with physical pain. This event-related fMRI study aims to compare the brain activity related to perceiving nociceptive pain and that emerging from processing semantic pain, i.e., words related to either physical or social pain, in order to identify common and distinct neural substrates. Methods Thirty-four healthy women underwent two fMRI sessions each. In the Semantic session, participants were presented with positive words, negative pain-unrelated words, physical pain-related words, and social pain-related words. In the Nociceptive session, participants received cutaneous mechanical stimulations that could be either painful or not. During both sessions, participants were asked to rate the unpleasantness of each stimulus. Linguistic stimuli were also rated in terms of valence, arousal, pain relatedness, and pain intensity, immediately after the Semantic session. Results In the Nociceptive session, the ‘nociceptive stimuli’ vs. ‘non-nociceptive stimuli’ contrast revealed extensive activations in SI, SII, insula, cingulate cortex, thalamus, and dorsolateral prefrontal cortex. In the Semantic session, words associated with social pain, compared to negative pain-unrelated words, showed increased activity in most of the same areas, whereas words associated with physical pain, compared to negative pain-unrelated words, only activated the left supramarginal gyrus and partly the postcentral gyrus. Discussion Our results confirm that semantic pain partly shares the neural substrates of nociceptive pain. Specifically, social pain-related words activate a wide network of regions, mostly overlapping with those pertaining to the affective-motivational aspects of nociception, whereas physical pain-related words overlap with a small cluster including regions related to the sensory-discriminative aspects of nociception. However, most regions of overlap are differentially activated in different conditions.
  • Publisher: Lausanne: Frontiers Research Foundation
  • Language: English
  • Identifier: ISSN: 1662-453X
    ISSN: 1662-4548
    EISSN: 1662-453X
    DOI: 10.3389/fnins.2023.1234286
  • Source: Freely Accessible Journals
    PubMed Central
    ProQuest Central
    DOAJ Directory of Open Access Journals
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