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Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain
The perception of pain is shaped by somatosensory information about threat. However, pain is also influenced by an individual’s expectations. Such expectations can result in clinically relevant modulations and abnormalities of pain. In the brain, sensory information, expectations (predictions), and...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740684/ https://www.ncbi.nlm.nih.gov/pubmed/34983852 http://dx.doi.org/10.1073/pnas.2116616119 |
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author | Nickel, Moritz M. Tiemann, Laura Hohn, Vanessa D. May, Elisabeth S. Gil Ávila, Cristina Eippert, Falk Ploner, Markus |
author_facet | Nickel, Moritz M. Tiemann, Laura Hohn, Vanessa D. May, Elisabeth S. Gil Ávila, Cristina Eippert, Falk Ploner, Markus |
author_sort | Nickel, Moritz M. |
collection | PubMed |
description | The perception of pain is shaped by somatosensory information about threat. However, pain is also influenced by an individual’s expectations. Such expectations can result in clinically relevant modulations and abnormalities of pain. In the brain, sensory information, expectations (predictions), and discrepancies thereof (prediction errors) are signaled by an extended network of brain areas which generate evoked potentials and oscillatory responses at different latencies and frequencies. However, a comprehensive picture of how evoked and oscillatory brain responses signal sensory information, predictions, and prediction errors in the processing of pain is lacking so far. Here, we therefore applied brief painful stimuli to 48 healthy human participants and independently modulated sensory information (stimulus intensity) and expectations of pain intensity while measuring brain activity using electroencephalography (EEG). Pain ratings confirmed that pain intensity was shaped by both sensory information and expectations. In contrast, Bayesian analyses revealed that stimulus-induced EEG responses at different latencies (the N1, N2, and P2 components) and frequencies (alpha, beta, and gamma oscillations) were shaped by sensory information but not by expectations. Expectations, however, shaped alpha and beta oscillations before the painful stimuli. These findings indicate that commonly analyzed EEG responses to painful stimuli are more involved in signaling sensory information than in signaling expectations or mismatches of sensory information and expectations. Moreover, they indicate that the effects of expectations on pain are served by brain mechanisms which differ from those conveying effects of sensory information on pain. |
format | Online Article Text |
id | pubmed-8740684 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-87406842022-01-25 Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain Nickel, Moritz M. Tiemann, Laura Hohn, Vanessa D. May, Elisabeth S. Gil Ávila, Cristina Eippert, Falk Ploner, Markus Proc Natl Acad Sci U S A Biological Sciences The perception of pain is shaped by somatosensory information about threat. However, pain is also influenced by an individual’s expectations. Such expectations can result in clinically relevant modulations and abnormalities of pain. In the brain, sensory information, expectations (predictions), and discrepancies thereof (prediction errors) are signaled by an extended network of brain areas which generate evoked potentials and oscillatory responses at different latencies and frequencies. However, a comprehensive picture of how evoked and oscillatory brain responses signal sensory information, predictions, and prediction errors in the processing of pain is lacking so far. Here, we therefore applied brief painful stimuli to 48 healthy human participants and independently modulated sensory information (stimulus intensity) and expectations of pain intensity while measuring brain activity using electroencephalography (EEG). Pain ratings confirmed that pain intensity was shaped by both sensory information and expectations. In contrast, Bayesian analyses revealed that stimulus-induced EEG responses at different latencies (the N1, N2, and P2 components) and frequencies (alpha, beta, and gamma oscillations) were shaped by sensory information but not by expectations. Expectations, however, shaped alpha and beta oscillations before the painful stimuli. These findings indicate that commonly analyzed EEG responses to painful stimuli are more involved in signaling sensory information than in signaling expectations or mismatches of sensory information and expectations. Moreover, they indicate that the effects of expectations on pain are served by brain mechanisms which differ from those conveying effects of sensory information on pain. National Academy of Sciences 2021-12-30 2022-01-04 /pmc/articles/PMC8740684/ /pubmed/34983852 http://dx.doi.org/10.1073/pnas.2116616119 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Nickel, Moritz M. Tiemann, Laura Hohn, Vanessa D. May, Elisabeth S. Gil Ávila, Cristina Eippert, Falk Ploner, Markus Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
title | Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
title_full | Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
title_fullStr | Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
title_full_unstemmed | Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
title_short | Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
title_sort | temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740684/ https://www.ncbi.nlm.nih.gov/pubmed/34983852 http://dx.doi.org/10.1073/pnas.2116616119 |
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