The expectations humans have of a pleasurable sensation asymmetrically shape neuronal responses and subjective experiences to hot sauce.

IF 9.8 1区 生物学 Q1 Agricultural and Biological Sciences
PLoS Biology Pub Date : 2024-10-08 eCollection Date: 2024-10-01 DOI:10.1371/journal.pbio.3002818
Yi Luo, Terry Lohrenz, Ellen A Lumpkin, P Read Montague, Kenneth T Kishida
{"title":"The expectations humans have of a pleasurable sensation asymmetrically shape neuronal responses and subjective experiences to hot sauce.","authors":"Yi Luo, Terry Lohrenz, Ellen A Lumpkin, P Read Montague, Kenneth T Kishida","doi":"10.1371/journal.pbio.3002818","DOIUrl":null,"url":null,"abstract":"<p><p>Expectations shape our perception, profoundly influencing how we interpret the world. Positive expectations about sensory stimuli can alleviate distress and reduce pain (e.g., placebo effect), while negative expectations may heighten anxiety and exacerbate pain (e.g., nocebo effect). To investigate the impact of the (an)hedonic aspect of expectations on subjective experiences, we measured neurobehavioral responses to the taste of hot sauce among participants with heterogeneous taste preferences. By identifying participants who \"liked\" versus those who strongly \"disliked\" spicy flavors and by providing contextual cues about the spiciness of the sauce to be tasted, we dissociated the effects of positive and negative expectations from sensory stimuli (i.e., visual and gustatory stimuli), which were the same across all participants. Our results indicate that positive expectations lead to modulations in the intensity of subjective experience. These modulations were accompanied by increased activity in brain regions previously linked to information integration and the placebo effect, including the anterior insula, dorsolateral prefrontal cortex, and dorsal anterior cingulate cortex, as well as a predefined \"pleasure signature.\" In contrast, negative expectations decreased hedonic experience and increased neural activity in the previously validated \"Neurological Pain Signature\" network. These findings demonstrate that hedonic aspects of one's expectations asymmetrically shape how the brain processes sensory input and associated behavioral reports of one's subjective experiences of intensity, pleasure, and pain. Our results suggest a dissociable impact of hedonic information: positive expectations facilitate higher-level information integration and reward processing, while negative expectations prime lower-level nociceptive and affective processes. This study demonstrates the powerful role of hedonic expectations in shaping subjective reality and suggests potential avenues for consumer and therapeutic interventions targeting expectation-driven neural processes.</p>","PeriodicalId":49001,"journal":{"name":"PLoS Biology","volume":"22 10","pages":"e3002818"},"PeriodicalIF":9.8000,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11460714/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pbio.3002818","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
引用次数: 0

Abstract

Expectations shape our perception, profoundly influencing how we interpret the world. Positive expectations about sensory stimuli can alleviate distress and reduce pain (e.g., placebo effect), while negative expectations may heighten anxiety and exacerbate pain (e.g., nocebo effect). To investigate the impact of the (an)hedonic aspect of expectations on subjective experiences, we measured neurobehavioral responses to the taste of hot sauce among participants with heterogeneous taste preferences. By identifying participants who "liked" versus those who strongly "disliked" spicy flavors and by providing contextual cues about the spiciness of the sauce to be tasted, we dissociated the effects of positive and negative expectations from sensory stimuli (i.e., visual and gustatory stimuli), which were the same across all participants. Our results indicate that positive expectations lead to modulations in the intensity of subjective experience. These modulations were accompanied by increased activity in brain regions previously linked to information integration and the placebo effect, including the anterior insula, dorsolateral prefrontal cortex, and dorsal anterior cingulate cortex, as well as a predefined "pleasure signature." In contrast, negative expectations decreased hedonic experience and increased neural activity in the previously validated "Neurological Pain Signature" network. These findings demonstrate that hedonic aspects of one's expectations asymmetrically shape how the brain processes sensory input and associated behavioral reports of one's subjective experiences of intensity, pleasure, and pain. Our results suggest a dissociable impact of hedonic information: positive expectations facilitate higher-level information integration and reward processing, while negative expectations prime lower-level nociceptive and affective processes. This study demonstrates the powerful role of hedonic expectations in shaping subjective reality and suggests potential avenues for consumer and therapeutic interventions targeting expectation-driven neural processes.

人类对愉悦感觉的期望不对称地影响着神经元对辣酱的反应和主观体验。
期望塑造我们的感知,深刻影响我们对世界的解读。对感官刺激的积极预期可以减轻痛苦和减轻疼痛(如安慰剂效应),而消极预期则可能会加剧焦虑和加重疼痛(如安慰剂效应)。为了研究期望的(享乐)方面对主观体验的影响,我们测量了具有不同口味偏好的参与者对辣酱味道的神经行为反应。通过鉴别 "喜欢 "辣味和强烈 "不喜欢 "辣味的参与者,以及提供有关将要品尝的调味汁辣度的情境线索,我们从感官刺激(即视觉和味觉刺激)中分离出了积极和消极期望的影响,这些影响在所有参与者中都是相同的。我们的研究结果表明,积极预期会导致主观体验强度的调节。这些调节伴随着先前与信息整合和安慰剂效应有关的脑区活动的增加,包括前脑岛、背外侧前额叶皮层和背侧前扣带回皮层,以及预先定义的 "愉悦特征"。与此相反,负面期望会减少享乐体验,并增加先前验证的 "神经疼痛特征 "网络的神经活动。这些研究结果表明,一个人对享乐方面的期望会不对称地影响大脑对感觉输入的处理,以及对强度、快乐和痛苦等主观体验的相关行为报告。我们的研究结果表明,享乐信息会产生不同的影响:积极的期望会促进较高层次的信息整合和奖赏处理,而消极的期望则会刺激较低层次的痛觉和情感过程。这项研究证明了享乐期望在塑造主观现实中的强大作用,并为针对期望驱动的神经过程的消费者和治疗干预提出了潜在的途径。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
PLoS Biology
PLoS Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-BIOLOGY
CiteScore
15.40
自引率
2.00%
发文量
359
审稿时长
3-8 weeks
期刊介绍: PLOS Biology is the flagship journal of the Public Library of Science (PLOS) and focuses on publishing groundbreaking and relevant research in all areas of biological science. The journal features works at various scales, ranging from molecules to ecosystems, and also encourages interdisciplinary studies. PLOS Biology publishes articles that demonstrate exceptional significance, originality, and relevance, with a high standard of scientific rigor in methodology, reporting, and conclusions. The journal aims to advance science and serve the research community by transforming research communication to align with the research process. It offers evolving article types and policies that empower authors to share the complete story behind their scientific findings with a diverse global audience of researchers, educators, policymakers, patient advocacy groups, and the general public. PLOS Biology, along with other PLOS journals, is widely indexed by major services such as Crossref, Dimensions, DOAJ, Google Scholar, PubMed, PubMed Central, Scopus, and Web of Science. Additionally, PLOS Biology is indexed by various other services including AGRICOLA, Biological Abstracts, BIOSYS Previews, CABI CAB Abstracts, CABI Global Health, CAPES, CAS, CNKI, Embase, Journal Guide, MEDLINE, and Zoological Record, ensuring that the research content is easily accessible and discoverable by a wide range of audiences.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信