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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...

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Autores principales: Nickel, Moritz M., Tiemann, Laura, Hohn, Vanessa D., May, Elisabeth S., Gil Ávila, Cristina, Eippert, Falk, Ploner, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
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.
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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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