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Temporal dynamics of fMRI signal changes during conditioned interoceptive pain-related fear and safety acquisition and extinction.
Behav Brain Res. 2022 06 03; 427:113868.BB

Abstract

Associative learning and memory mechanisms drive interoceptive signaling along the gut-brain axis, thus shaping affective-emotional reactions and behavior. Specifically, learning to predict potentially harmful, visceral pain is assumed to succeed within very few trials. However, the temporal dynamics of cerebellar and cerebral fMRI signal changes underlying early acquisition and extinction of learned fear signals and the concomitant evolvement of safety learning remain incompletely understood. 3 T fMRI data of healthy individuals from three studies were uniformly processed across the whole brain and the cerebellum. All studies employed differential delay conditioning (N = 94) with one visual cue (CS+) being repeatedly paired with visceral pain as unconditioned stimulus (US) while a second cue remained unpaired (CS-). During subsequent extinction (N = 51), all CS were presented without US. Behavioral results revealed increased CS+-aversiveness and CS--pleasantness after conditioning and diminished valence ratings for both CS following extinction. During early acquisition, the CS- induced linearly increasing neural activation in the insula, midcingulate cortex, hippocampus, precuneus as well as cerebral and cerebellar somatomotor regions. The comparison between acquisition and extinction phases yielded a CS--induced linear increase in the posterior cingulate cortex and precuneus during early acquisition, while there was no evidence for linear fMRI signal changes for the CS+ during acquisition and for both CS during extinction. Based on theoretical accounts of discrimination and temporal difference learning, these results suggest a gradual evolvement of learned safety cues that engage emotional arousal, memory, and cortical modulatory networks. As safety signals are presumably more difficult to learn and to discriminate from learned threat cues, the underlying temporal dynamics may reflect enhanced salience and prediction processing as well as increasing demands for attentional resources and the integration of multisensory information. Maladaptive responses to learned safety signals are a clinically relevant phenotype in multiple conditions, including chronic visceral pain, and can be exceptionally resistant to modification or extinction. Through sustained hypervigilance, safety seeking constitutes one key component in pain and stress-related avoidance behavior, calling for future studies targeting the mechanisms of safety learning and extinction to advance current cognitive-behavioral treatment approaches.

Authors+Show Affiliations

Department of Medical Psychology and Medical Sociology, Faculty of Medicine, Ruhr University Bochum, Bochum, Germany; Department of Neurology, Center for Translational Neuro, and Behavioral Sciences (C-TNBS), University Hospital Essen, University of Duisburg-Essen, Essen, Germany. Electronic address: franziska.labrenz@ruhr-uni-bochum.de.Institute of Diagnostic and Interventional Radiology and Neuroradiology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.Department of Neurology, Center for Translational Neuro, and Behavioral Sciences (C-TNBS), University Hospital Essen, University of Duisburg-Essen, Essen, Germany.Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Bochum, Germany.High-Field and Hybrid Magnetic Resonance Imaging, University Hospital Essen, Essen, Germany; Erwin L. Hahn Institute for MR Imaging, University of Duisburg-Essen, Essen, Germany.Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Bochum, Germany.Department of Medical Psychology and Medical Sociology, Faculty of Medicine, Ruhr University Bochum, Bochum, Germany; Department of Neurology, Center for Translational Neuro, and Behavioral Sciences (C-TNBS), University Hospital Essen, University of Duisburg-Essen, Essen, Germany.Department of Neurology, Center for Translational Neuro, and Behavioral Sciences (C-TNBS), University Hospital Essen, University of Duisburg-Essen, Essen, Germany.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

35364111

Citation

Labrenz, Franziska, et al. "Temporal Dynamics of fMRI Signal Changes During Conditioned Interoceptive Pain-related Fear and Safety Acquisition and Extinction." Behavioural Brain Research, vol. 427, 2022, p. 113868.
Labrenz F, Spisák T, Ernst TM, et al. Temporal dynamics of fMRI signal changes during conditioned interoceptive pain-related fear and safety acquisition and extinction. Behav Brain Res. 2022;427:113868.
Labrenz, F., Spisák, T., Ernst, T. M., Gomes, C. A., Quick, H. H., Axmacher, N., Elsenbruch, S., & Timmann, D. (2022). Temporal dynamics of fMRI signal changes during conditioned interoceptive pain-related fear and safety acquisition and extinction. Behavioural Brain Research, 427, 113868. https://doi.org/10.1016/j.bbr.2022.113868
Labrenz F, et al. Temporal Dynamics of fMRI Signal Changes During Conditioned Interoceptive Pain-related Fear and Safety Acquisition and Extinction. Behav Brain Res. 2022 06 3;427:113868. PubMed PMID: 35364111.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Temporal dynamics of fMRI signal changes during conditioned interoceptive pain-related fear and safety acquisition and extinction. AU - Labrenz,Franziska, AU - Spisák,Tamás, AU - Ernst,Thomas M, AU - Gomes,Carlos A, AU - Quick,Harald H, AU - Axmacher,Nikolai, AU - Elsenbruch,Sigrid, AU - Timmann,Dagmar, Y1 - 2022/03/29/ PY - 2021/10/19/received PY - 2022/03/14/revised PY - 2022/03/28/accepted PY - 2022/4/2/pubmed PY - 2022/4/21/medline PY - 2022/4/1/entrez KW - Differential fear conditioning KW - FMRI KW - Gut-brain axis KW - Pain-related fear KW - Safety learning KW - Temporal dynamics SP - 113868 EP - 113868 JF - Behavioural brain research JO - Behav Brain Res VL - 427 N2 - Associative learning and memory mechanisms drive interoceptive signaling along the gut-brain axis, thus shaping affective-emotional reactions and behavior. Specifically, learning to predict potentially harmful, visceral pain is assumed to succeed within very few trials. However, the temporal dynamics of cerebellar and cerebral fMRI signal changes underlying early acquisition and extinction of learned fear signals and the concomitant evolvement of safety learning remain incompletely understood. 3 T fMRI data of healthy individuals from three studies were uniformly processed across the whole brain and the cerebellum. All studies employed differential delay conditioning (N = 94) with one visual cue (CS+) being repeatedly paired with visceral pain as unconditioned stimulus (US) while a second cue remained unpaired (CS-). During subsequent extinction (N = 51), all CS were presented without US. Behavioral results revealed increased CS+-aversiveness and CS--pleasantness after conditioning and diminished valence ratings for both CS following extinction. During early acquisition, the CS- induced linearly increasing neural activation in the insula, midcingulate cortex, hippocampus, precuneus as well as cerebral and cerebellar somatomotor regions. The comparison between acquisition and extinction phases yielded a CS--induced linear increase in the posterior cingulate cortex and precuneus during early acquisition, while there was no evidence for linear fMRI signal changes for the CS+ during acquisition and for both CS during extinction. Based on theoretical accounts of discrimination and temporal difference learning, these results suggest a gradual evolvement of learned safety cues that engage emotional arousal, memory, and cortical modulatory networks. As safety signals are presumably more difficult to learn and to discriminate from learned threat cues, the underlying temporal dynamics may reflect enhanced salience and prediction processing as well as increasing demands for attentional resources and the integration of multisensory information. Maladaptive responses to learned safety signals are a clinically relevant phenotype in multiple conditions, including chronic visceral pain, and can be exceptionally resistant to modification or extinction. Through sustained hypervigilance, safety seeking constitutes one key component in pain and stress-related avoidance behavior, calling for future studies targeting the mechanisms of safety learning and extinction to advance current cognitive-behavioral treatment approaches. SN - 1872-7549 UR - https://www.unboundmedicine.com/medline/citation/35364111/Temporal_dynamics_of_fMRI_signal_changes_during_conditioned_interoceptive_pain_related_fear_and_safety_acquisition_and_extinction_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0166-4328(22)00136-X DB - PRIME DP - Unbound Medicine ER -