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Relief as a Reward: Hedonic and Neural Responses to Safety from Pain

Relief fits the definition of a reward. Unlike other reward types the pleasantness of relief depends on the violation of a negative expectation, yet this has not been investigated using neuroimaging approaches. We hypothesized that the degree of negative expectation depends on state (dread) and trai...

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Autores principales: Leknes, Siri, Lee, Michael, Berna, Chantal, Andersson, Jesper, Tracey, Irene
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3072382/
https://www.ncbi.nlm.nih.gov/pubmed/21490964
http://dx.doi.org/10.1371/journal.pone.0017870
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author Leknes, Siri
Lee, Michael
Berna, Chantal
Andersson, Jesper
Tracey, Irene
author_facet Leknes, Siri
Lee, Michael
Berna, Chantal
Andersson, Jesper
Tracey, Irene
author_sort Leknes, Siri
collection PubMed
description Relief fits the definition of a reward. Unlike other reward types the pleasantness of relief depends on the violation of a negative expectation, yet this has not been investigated using neuroimaging approaches. We hypothesized that the degree of negative expectation depends on state (dread) and trait (pessimism) sensitivity. Of the brain regions that are involved in mediating pleasure, the nucleus accumbens also signals unexpected reward and positive prediction error. We hypothesized that accumbens activity reflects the level of negative expectation and subsequent pleasant relief. Using fMRI and two purpose-made tasks, we compared hedonic and BOLD responses to relief with responses during an appetitive reward task in 18 healthy volunteers. We expected some similarities in task responses, reflecting common neural substrates implicated across reward types. However, we also hypothesized that relief responses would differ from appetitive rewards in the nucleus accumbens, since only relief pleasantness depends on negative expectations. The results confirmed these hypotheses. Relief and appetitive reward task activity converged in the ventromedial prefrontal cortex, which also correlated with appetitive reward pleasantness ratings. In contrast, dread and pessimism scores correlated with relief but not with appetitive reward hedonics. Moreover, only relief pleasantness covaried with accumbens activation. Importantly, the accumbens signal appeared to specifically reflect individual differences in anticipation of the adverse event (dread, pessimism) but was uncorrelated to appetitive reward hedonics. In conclusion, relief differs from appetitive rewards due to its reliance on negative expectations, the violation of which is reflected in relief-related accumbens activation.
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spelling pubmed-30723822011-04-13 Relief as a Reward: Hedonic and Neural Responses to Safety from Pain Leknes, Siri Lee, Michael Berna, Chantal Andersson, Jesper Tracey, Irene PLoS One Research Article Relief fits the definition of a reward. Unlike other reward types the pleasantness of relief depends on the violation of a negative expectation, yet this has not been investigated using neuroimaging approaches. We hypothesized that the degree of negative expectation depends on state (dread) and trait (pessimism) sensitivity. Of the brain regions that are involved in mediating pleasure, the nucleus accumbens also signals unexpected reward and positive prediction error. We hypothesized that accumbens activity reflects the level of negative expectation and subsequent pleasant relief. Using fMRI and two purpose-made tasks, we compared hedonic and BOLD responses to relief with responses during an appetitive reward task in 18 healthy volunteers. We expected some similarities in task responses, reflecting common neural substrates implicated across reward types. However, we also hypothesized that relief responses would differ from appetitive rewards in the nucleus accumbens, since only relief pleasantness depends on negative expectations. The results confirmed these hypotheses. Relief and appetitive reward task activity converged in the ventromedial prefrontal cortex, which also correlated with appetitive reward pleasantness ratings. In contrast, dread and pessimism scores correlated with relief but not with appetitive reward hedonics. Moreover, only relief pleasantness covaried with accumbens activation. Importantly, the accumbens signal appeared to specifically reflect individual differences in anticipation of the adverse event (dread, pessimism) but was uncorrelated to appetitive reward hedonics. In conclusion, relief differs from appetitive rewards due to its reliance on negative expectations, the violation of which is reflected in relief-related accumbens activation. Public Library of Science 2011-04-07 /pmc/articles/PMC3072382/ /pubmed/21490964 http://dx.doi.org/10.1371/journal.pone.0017870 Text en Leknes et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Leknes, Siri
Lee, Michael
Berna, Chantal
Andersson, Jesper
Tracey, Irene
Relief as a Reward: Hedonic and Neural Responses to Safety from Pain
title Relief as a Reward: Hedonic and Neural Responses to Safety from Pain
title_full Relief as a Reward: Hedonic and Neural Responses to Safety from Pain
title_fullStr Relief as a Reward: Hedonic and Neural Responses to Safety from Pain
title_full_unstemmed Relief as a Reward: Hedonic and Neural Responses to Safety from Pain
title_short Relief as a Reward: Hedonic and Neural Responses to Safety from Pain
title_sort relief as a reward: hedonic and neural responses to safety from pain
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3072382/
https://www.ncbi.nlm.nih.gov/pubmed/21490964
http://dx.doi.org/10.1371/journal.pone.0017870
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