The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm

Prediction errors are thought to drive associative fear learning. Surprisingly little is known about the possible contribution of the cerebellum. To address this question, healthy participants underwent a differential fear conditioning paradigm during 7T magnetic resonance imaging. An event-related...

Full description

Bibliographic Details
Main Authors: Thomas Michael Ernst, Anna Evelina Brol, Marcel Gratz, Christoph Ritter, Ulrike Bingel, Marc Schlamann, Stefan Maderwald, Harald H Quick, Christian Josef Merz, Dagmar Timmann
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/46831
_version_ 1811181446463750144
author Thomas Michael Ernst
Anna Evelina Brol
Marcel Gratz
Christoph Ritter
Ulrike Bingel
Marc Schlamann
Stefan Maderwald
Harald H Quick
Christian Josef Merz
Dagmar Timmann
author_facet Thomas Michael Ernst
Anna Evelina Brol
Marcel Gratz
Christoph Ritter
Ulrike Bingel
Marc Schlamann
Stefan Maderwald
Harald H Quick
Christian Josef Merz
Dagmar Timmann
author_sort Thomas Michael Ernst
collection DOAJ
description Prediction errors are thought to drive associative fear learning. Surprisingly little is known about the possible contribution of the cerebellum. To address this question, healthy participants underwent a differential fear conditioning paradigm during 7T magnetic resonance imaging. An event-related design allowed us to separate cerebellar fMRI signals related to the visual conditioned stimulus (CS) from signals related to the subsequent unconditioned stimulus (US; an aversive electric shock). We found significant activation of cerebellar lobules Crus I and VI bilaterally related to the CS+ compared to the CS-. Most importantly, significant activation of lobules Crus I and VI was also present during the unexpected omission of the US in unreinforced CS+ acquisition trials. This activation disappeared during extinction when US omission became expected. These findings provide evidence that the cerebellum has to be added to the neural network processing predictions and prediction errors in the emotional domain.
first_indexed 2024-04-11T09:17:52Z
format Article
id doaj.art-30761d716c7145b3aa0e53a6a95f0c35
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T09:17:52Z
publishDate 2019-08-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-30761d716c7145b3aa0e53a6a95f0c352022-12-22T04:32:17ZengeLife Sciences Publications LtdeLife2050-084X2019-08-01810.7554/eLife.46831The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigmThomas Michael Ernst0https://orcid.org/0000-0002-2170-9241Anna Evelina Brol1Marcel Gratz2Christoph Ritter3Ulrike Bingel4Marc Schlamann5Stefan Maderwald6Harald H Quick7Christian Josef Merz8Dagmar Timmann9Department of Neurology, Essen University Hospital, Essen, Germany; Erwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyDepartment of Neurology, Essen University Hospital, Essen, GermanyErwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, Germany; High-Field and Hybrid MR Imaging, Essen University Hospital, Essen, GermanyDepartment of Neurology, Essen University Hospital, Essen, GermanyDepartment of Neurology, Essen University Hospital, Essen, GermanyInstitute of Diagnostic and Interventional Radiology and Neuroradiology, Essen University Hospital, Essen, Germany; Department of Neuroradiology, University Hospital Cologne, Cologne, GermanyErwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyErwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, Germany; High-Field and Hybrid MR Imaging, Essen University Hospital, Essen, GermanyDepartment of Cognitive Psychology, Institute of Cognitive Neuroscience, Ruhr University Bochum, Bochum, GermanyDepartment of Neurology, Essen University Hospital, Essen, Germany; Erwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyPrediction errors are thought to drive associative fear learning. Surprisingly little is known about the possible contribution of the cerebellum. To address this question, healthy participants underwent a differential fear conditioning paradigm during 7T magnetic resonance imaging. An event-related design allowed us to separate cerebellar fMRI signals related to the visual conditioned stimulus (CS) from signals related to the subsequent unconditioned stimulus (US; an aversive electric shock). We found significant activation of cerebellar lobules Crus I and VI bilaterally related to the CS+ compared to the CS-. Most importantly, significant activation of lobules Crus I and VI was also present during the unexpected omission of the US in unreinforced CS+ acquisition trials. This activation disappeared during extinction when US omission became expected. These findings provide evidence that the cerebellum has to be added to the neural network processing predictions and prediction errors in the emotional domain.https://elifesciences.org/articles/46831emotionsextinctionfearvermiscerebellar hemisphereaversive conditioning
spellingShingle Thomas Michael Ernst
Anna Evelina Brol
Marcel Gratz
Christoph Ritter
Ulrike Bingel
Marc Schlamann
Stefan Maderwald
Harald H Quick
Christian Josef Merz
Dagmar Timmann
The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
eLife
emotions
extinction
fear
vermis
cerebellar hemisphere
aversive conditioning
title The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
title_full The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
title_fullStr The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
title_full_unstemmed The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
title_short The cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
title_sort cerebellum is involved in processing of predictions and prediction errors in a fear conditioning paradigm
topic emotions
extinction
fear
vermis
cerebellar hemisphere
aversive conditioning
url https://elifesciences.org/articles/46831
work_keys_str_mv AT thomasmichaelernst thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT annaevelinabrol thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT marcelgratz thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT christophritter thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT ulrikebingel thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT marcschlamann thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT stefanmaderwald thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT haraldhquick thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT christianjosefmerz thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT dagmartimmann thecerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT thomasmichaelernst cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT annaevelinabrol cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT marcelgratz cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT christophritter cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT ulrikebingel cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT marcschlamann cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT stefanmaderwald cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT haraldhquick cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT christianjosefmerz cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm
AT dagmartimmann cerebellumisinvolvedinprocessingofpredictionsandpredictionerrorsinafearconditioningparadigm