Carolina Ceruti, Laura Petrini, Giulia Erica Aliotta, Dennis Boye Larsen, Elia Valentini, Kristian Hennings, Carina Graversen, Carsten Dahl Mørch
{"title":"在操作性学习过程中,对疼痛的预期会增加认知表现和反馈相关的皮质电位。","authors":"Carolina Ceruti, Laura Petrini, Giulia Erica Aliotta, Dennis Boye Larsen, Elia Valentini, Kristian Hennings, Carina Graversen, Carsten Dahl Mørch","doi":"10.1007/s00221-025-07167-9","DOIUrl":null,"url":null,"abstract":"<p><p>Operant conditioning (OC) evokes behavioral changes and may be useful in pain management. However, it is unknown how alteration of a tonic painful stimulus may affect cognitive performance in an OC learning task and the associated neural activity. To address this, specific event-related potentials (ERPs) and cognitive performance were assessed after an OC task, using altered pain intensity as the operant stimulus. Two OC paradigms were designed using painful tonic pressure pain as the conditioning stimulus. 29 healthy participants received individually set tonic pressure pain corresponding to visual analogue scale 5 (VAS5; pain threshold). Pressure was maintained and a cognitive task performance yielded reward or punishment. Consequences of correct and incorrect answers in the negative reinforcement (NR) condition were pain relief (VAS3) or no pressure change (VAS5), respectively, and no pressure change (VAS5) or increased pressure (VAS7) in the positive punishment (PP) condition, respectively. The initial condition (NR or PP) was randomized, and 120 trials were conducted in three same-day sessions. 64-channel electroencephalography was recorded, and auditory-feedback ERPs (P1N1, P2N2, P3N3) were extracted. Higher ERP peak-to-peak amplitudes were found when participants received feedback that their answer was incorrect. A small OC learning behavior effect was found across trials with no difference between NR and PP. Independent of OC paradigm, learning behavior was induced, and ERP complex amplitudes increased when incorrect answers were given. These novel findings show that higher pain expectancy due to an incorrect answer, facilitated feedback-related ERPs when using pain as a conditioning stimulus.</p>","PeriodicalId":12268,"journal":{"name":"Experimental Brain Research","volume":"243 11","pages":"221"},"PeriodicalIF":1.6000,"publicationDate":"2025-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12496262/pdf/","citationCount":"0","resultStr":"{\"title\":\"Anticipation of pain during operant learning increases cognitive performance and feedback-related cortical potentials.\",\"authors\":\"Carolina Ceruti, Laura Petrini, Giulia Erica Aliotta, Dennis Boye Larsen, Elia Valentini, Kristian Hennings, Carina Graversen, Carsten Dahl Mørch\",\"doi\":\"10.1007/s00221-025-07167-9\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Operant conditioning (OC) evokes behavioral changes and may be useful in pain management. However, it is unknown how alteration of a tonic painful stimulus may affect cognitive performance in an OC learning task and the associated neural activity. To address this, specific event-related potentials (ERPs) and cognitive performance were assessed after an OC task, using altered pain intensity as the operant stimulus. Two OC paradigms were designed using painful tonic pressure pain as the conditioning stimulus. 29 healthy participants received individually set tonic pressure pain corresponding to visual analogue scale 5 (VAS5; pain threshold). Pressure was maintained and a cognitive task performance yielded reward or punishment. Consequences of correct and incorrect answers in the negative reinforcement (NR) condition were pain relief (VAS3) or no pressure change (VAS5), respectively, and no pressure change (VAS5) or increased pressure (VAS7) in the positive punishment (PP) condition, respectively. The initial condition (NR or PP) was randomized, and 120 trials were conducted in three same-day sessions. 64-channel electroencephalography was recorded, and auditory-feedback ERPs (P1N1, P2N2, P3N3) were extracted. Higher ERP peak-to-peak amplitudes were found when participants received feedback that their answer was incorrect. A small OC learning behavior effect was found across trials with no difference between NR and PP. Independent of OC paradigm, learning behavior was induced, and ERP complex amplitudes increased when incorrect answers were given. These novel findings show that higher pain expectancy due to an incorrect answer, facilitated feedback-related ERPs when using pain as a conditioning stimulus.</p>\",\"PeriodicalId\":12268,\"journal\":{\"name\":\"Experimental Brain Research\",\"volume\":\"243 11\",\"pages\":\"221\"},\"PeriodicalIF\":1.6000,\"publicationDate\":\"2025-10-04\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12496262/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Experimental Brain Research\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1007/s00221-025-07167-9\",\"RegionNum\":4,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q4\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Experimental Brain Research","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1007/s00221-025-07167-9","RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q4","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Anticipation of pain during operant learning increases cognitive performance and feedback-related cortical potentials.
Operant conditioning (OC) evokes behavioral changes and may be useful in pain management. However, it is unknown how alteration of a tonic painful stimulus may affect cognitive performance in an OC learning task and the associated neural activity. To address this, specific event-related potentials (ERPs) and cognitive performance were assessed after an OC task, using altered pain intensity as the operant stimulus. Two OC paradigms were designed using painful tonic pressure pain as the conditioning stimulus. 29 healthy participants received individually set tonic pressure pain corresponding to visual analogue scale 5 (VAS5; pain threshold). Pressure was maintained and a cognitive task performance yielded reward or punishment. Consequences of correct and incorrect answers in the negative reinforcement (NR) condition were pain relief (VAS3) or no pressure change (VAS5), respectively, and no pressure change (VAS5) or increased pressure (VAS7) in the positive punishment (PP) condition, respectively. The initial condition (NR or PP) was randomized, and 120 trials were conducted in three same-day sessions. 64-channel electroencephalography was recorded, and auditory-feedback ERPs (P1N1, P2N2, P3N3) were extracted. Higher ERP peak-to-peak amplitudes were found when participants received feedback that their answer was incorrect. A small OC learning behavior effect was found across trials with no difference between NR and PP. Independent of OC paradigm, learning behavior was induced, and ERP complex amplitudes increased when incorrect answers were given. These novel findings show that higher pain expectancy due to an incorrect answer, facilitated feedback-related ERPs when using pain as a conditioning stimulus.
期刊介绍:
Founded in 1966, Experimental Brain Research publishes original contributions on many aspects of experimental research of the central and peripheral nervous system. The focus is on molecular, physiology, behavior, neurochemistry, developmental, cellular and molecular neurobiology, and experimental pathology relevant to general problems of cerebral function. The journal publishes original papers, reviews, and mini-reviews.