The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study
The cerebellum is involved in the acquisition and consolidation of learned fear responses. Knowledge about its contribution to extinction learning, however, is sparse. Extinction processes likely involve erasure of memories, but there is ample evidence that at least part of the original memory remai...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-06-01
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| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922002099 |
| _version_ | 1818774476699992064 |
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| author | Giorgi Batsikadze Nicolas Diekmann Thomas Michael Ernst Michael Klein Stefan Maderwald Cornelius Deuschl Christian Josef Merz Sen Cheng Harald H. Quick Dagmar Timmann |
| author_facet | Giorgi Batsikadze Nicolas Diekmann Thomas Michael Ernst Michael Klein Stefan Maderwald Cornelius Deuschl Christian Josef Merz Sen Cheng Harald H. Quick Dagmar Timmann |
| author_sort | Giorgi Batsikadze |
| collection | DOAJ |
| description | The cerebellum is involved in the acquisition and consolidation of learned fear responses. Knowledge about its contribution to extinction learning, however, is sparse. Extinction processes likely involve erasure of memories, but there is ample evidence that at least part of the original memory remains. We asked the question whether memory persists within the cerebellum following extinction training. The renewal effect, that is the reoccurrence of the extinguished fear memory during recall in a context different from the extinction context, constitutes one of the phenomena indicating that memory of extinguished learned fear responses is not fully erased during extinction training. We performed a differential AB-A/B fear conditioning paradigm in a 7-Tesla (7T) MRI system in 31 young and healthy men. On day 1, fear acquisition training was performed in context A and extinction training in context B. On day 2, recall was tested in contexts A and B. As expected, participants learned to predict that the CS+ was followed by an aversive electric shock during fear acquisition training. Skin conductance responses (SCRs) were significantly higher to the CS+ compared to the CS- at the end of acquisition. Differences in SCRs vanished in extinction and reoccurred in the acquisition context during recall indicating renewal. Fitting SCR data, a deep neural network model was trained to predict the correct shock value for a given stimulus and context. Event-related fMRI analysis with model-derived prediction values as parametric modulations showed significant effects on activation of the posterolateral cerebellum (lobules VI and Crus I) during recall. Since the prediction values differ based on stimulus (CS+ and CS-) and context during recall, data provide support that the cerebellum is involved in context-related recall of learned fear associations. Likewise, mean β values were highest in lobules VI and Crus I bilaterally related to the CS+ in the acquisition context during early recall. A similar pattern was seen in the vermis, but only on a trend level. Thus, part of the original memory likely remains within the cerebellum following extinction training. We found cerebellar activations related to the CS+ and CS- during fear acquisition training which likely reflect associative and non-associative aspects of the task. Cerebellar activations, however, were not significantly different for CS+ and CS-. Since the CS- was never followed by an electric shock, the cerebellum may contribute to associative learning related to the CS, for example as a safety cue. |
| first_indexed | 2024-12-18T10:41:45Z |
| format | Article |
| id | doaj.art-b4b6492844f64b60a30c25a1692bfd18 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-18T10:41:45Z |
| publishDate | 2022-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-b4b6492844f64b60a30c25a1692bfd182022-12-21T21:10:38ZengElsevierNeuroImage1095-95722022-06-01253119080The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI studyGiorgi Batsikadze0Nicolas Diekmann1Thomas Michael Ernst2Michael Klein3Stefan Maderwald4Cornelius Deuschl5Christian Josef Merz6Sen Cheng7Harald H. Quick8Dagmar Timmann9Department of Neurology and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Hufelandstraße 55, Essen 45147, Germany; Corresponding author.Institute for Neural Computation, Ruhr University Bochum, Bochum, GermanyDepartment of Neurology and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Hufelandstraße 55, Essen 45147, Germany; Erwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyDepartment of Neurology and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Hufelandstraße 55, Essen 45147, GermanyErwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyInstitute of Diagnostic and Interventional Radiology and Neuroradiology, Essen University Hospital, Essen, GermanyDepartment of Cognitive Psychology, Institute of Cognitive Neuroscience, Ruhr University Bochum, Bochum, GermanyInstitute for Neural Computation, Ruhr University Bochum, Bochum, 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 and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Hufelandstraße 55, Essen 45147, Germany; Erwin L. Hahn Institute for Magnetic Resonance Imaging, University of Duisburg-Essen, Essen, GermanyThe cerebellum is involved in the acquisition and consolidation of learned fear responses. Knowledge about its contribution to extinction learning, however, is sparse. Extinction processes likely involve erasure of memories, but there is ample evidence that at least part of the original memory remains. We asked the question whether memory persists within the cerebellum following extinction training. The renewal effect, that is the reoccurrence of the extinguished fear memory during recall in a context different from the extinction context, constitutes one of the phenomena indicating that memory of extinguished learned fear responses is not fully erased during extinction training. We performed a differential AB-A/B fear conditioning paradigm in a 7-Tesla (7T) MRI system in 31 young and healthy men. On day 1, fear acquisition training was performed in context A and extinction training in context B. On day 2, recall was tested in contexts A and B. As expected, participants learned to predict that the CS+ was followed by an aversive electric shock during fear acquisition training. Skin conductance responses (SCRs) were significantly higher to the CS+ compared to the CS- at the end of acquisition. Differences in SCRs vanished in extinction and reoccurred in the acquisition context during recall indicating renewal. Fitting SCR data, a deep neural network model was trained to predict the correct shock value for a given stimulus and context. Event-related fMRI analysis with model-derived prediction values as parametric modulations showed significant effects on activation of the posterolateral cerebellum (lobules VI and Crus I) during recall. Since the prediction values differ based on stimulus (CS+ and CS-) and context during recall, data provide support that the cerebellum is involved in context-related recall of learned fear associations. Likewise, mean β values were highest in lobules VI and Crus I bilaterally related to the CS+ in the acquisition context during early recall. A similar pattern was seen in the vermis, but only on a trend level. Thus, part of the original memory likely remains within the cerebellum following extinction training. We found cerebellar activations related to the CS+ and CS- during fear acquisition training which likely reflect associative and non-associative aspects of the task. Cerebellar activations, however, were not significantly different for CS+ and CS-. Since the CS- was never followed by an electric shock, the cerebellum may contribute to associative learning related to the CS, for example as a safety cue.http://www.sciencedirect.com/science/article/pii/S1053811922002099Fear conditioningAcquisitionAssociative learningErasureInhibitory learningHuman |
| spellingShingle | Giorgi Batsikadze Nicolas Diekmann Thomas Michael Ernst Michael Klein Stefan Maderwald Cornelius Deuschl Christian Josef Merz Sen Cheng Harald H. Quick Dagmar Timmann The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study NeuroImage Fear conditioning Acquisition Associative learning Erasure Inhibitory learning Human |
| title | The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study |
| title_full | The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study |
| title_fullStr | The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study |
| title_full_unstemmed | The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study |
| title_short | The cerebellum contributes to context-effects during fear extinction learning: A 7T fMRI study |
| title_sort | cerebellum contributes to context effects during fear extinction learning a 7t fmri study |
| topic | Fear conditioning Acquisition Associative learning Erasure Inhibitory learning Human |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922002099 |
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