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Towards understanding sex differences in visceral pain: enhanced reactivation of classically-conditioned fear in healthy women.
Neurobiol Learn Mem. 2014 Mar; 109:113-21.NL

Abstract

Sex differences in learned fear regarding aversive gastrointestinal stimuli could play a role in the female preponderance of chronic abdominal pain. In a fear conditioning model with rectal pain as unconditioned stimulus (US), we compared healthy males and females with respect to neural responses during aversive visceral learning, extinction and re-activation of fear memory (i.e., reinstatement). To do so, conditioned visual stimuli (CS(+)) were consistently paired with painful rectal distensions as US, while different visual stimuli (CS(-)) were presented without US. During extinction, both CSs were presented without US, whereas during reinstatement, a single, unpaired US was presented. In region-of-interest analyses, sexes were compared with respect to conditioned anticipatory neural activation (CS(+)>CS(-)). The results revealed that in late acquisition, CS+ presentation induced significantly greater anticipatory activation of the insula in women. During extinction, women demonstrated reduced activation of the posterior cingulate cortex. During reinstatement, the CS(+) led to greater activation of the hippocampus, thalamus and cerebellum in women. These group effects in neural activation during learning and memory processes were not accounted for by sex differences in pain thresholds, pain ratings, or stress parameters. In conclusion, this is the first study to support sex differences in neural processes mediating aversive visceral learning. Our finding of enhanced neural responses during reinstatement in key brain areas relevant for memory suggests enhanced reactivation of old fear memory trace in women. Sex differences in "gut memories" could play a role in the female preponderance of chronic abdominal pain.

Authors+Show Affiliations

Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany.Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany.Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany; Institute of Diagnostic and Interventional Radiology and Neuroradiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany.Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany.Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany.Institute of Diagnostic and Interventional Radiology and Neuroradiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany.Clinic for Neuroradiology, Innsbruck Medical University, Innrain 52, A-6020 Innsbruck, Austria.Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, D-45147 Essen, Germany. Electronic address: sigrid.elsenbruch@uk-essen.de.

Pub Type(s)

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

Language

eng

PubMed ID

24398396

Citation

Benson, Sven, et al. "Towards Understanding Sex Differences in Visceral Pain: Enhanced Reactivation of Classically-conditioned Fear in Healthy Women." Neurobiology of Learning and Memory, vol. 109, 2014, pp. 113-21.
Benson S, Kattoor J, Kullmann JS, et al. Towards understanding sex differences in visceral pain: enhanced reactivation of classically-conditioned fear in healthy women. Neurobiol Learn Mem. 2014;109:113-21.
Benson, S., Kattoor, J., Kullmann, J. S., Hofmann, S., Engler, H., Forsting, M., Gizewski, E. R., & Elsenbruch, S. (2014). Towards understanding sex differences in visceral pain: enhanced reactivation of classically-conditioned fear in healthy women. Neurobiology of Learning and Memory, 109, 113-21. https://doi.org/10.1016/j.nlm.2013.12.014
Benson S, et al. Towards Understanding Sex Differences in Visceral Pain: Enhanced Reactivation of Classically-conditioned Fear in Healthy Women. Neurobiol Learn Mem. 2014;109:113-21. PubMed PMID: 24398396.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Towards understanding sex differences in visceral pain: enhanced reactivation of classically-conditioned fear in healthy women. AU - Benson,Sven, AU - Kattoor,Joswin, AU - Kullmann,Jennifer S, AU - Hofmann,Sarah, AU - Engler,Harald, AU - Forsting,Michael, AU - Gizewski,Elke R, AU - Elsenbruch,Sigrid, Y1 - 2014/01/04/ PY - 2013/09/10/received PY - 2013/12/19/revised PY - 2013/12/27/accepted PY - 2014/1/9/entrez PY - 2014/1/9/pubmed PY - 2014/10/31/medline KW - Brain imaging KW - Emotional memory KW - Fear conditioning KW - Sex differences KW - Visceral pain SP - 113 EP - 21 JF - Neurobiology of learning and memory JO - Neurobiol Learn Mem VL - 109 N2 - Sex differences in learned fear regarding aversive gastrointestinal stimuli could play a role in the female preponderance of chronic abdominal pain. In a fear conditioning model with rectal pain as unconditioned stimulus (US), we compared healthy males and females with respect to neural responses during aversive visceral learning, extinction and re-activation of fear memory (i.e., reinstatement). To do so, conditioned visual stimuli (CS(+)) were consistently paired with painful rectal distensions as US, while different visual stimuli (CS(-)) were presented without US. During extinction, both CSs were presented without US, whereas during reinstatement, a single, unpaired US was presented. In region-of-interest analyses, sexes were compared with respect to conditioned anticipatory neural activation (CS(+)>CS(-)). The results revealed that in late acquisition, CS+ presentation induced significantly greater anticipatory activation of the insula in women. During extinction, women demonstrated reduced activation of the posterior cingulate cortex. During reinstatement, the CS(+) led to greater activation of the hippocampus, thalamus and cerebellum in women. These group effects in neural activation during learning and memory processes were not accounted for by sex differences in pain thresholds, pain ratings, or stress parameters. In conclusion, this is the first study to support sex differences in neural processes mediating aversive visceral learning. Our finding of enhanced neural responses during reinstatement in key brain areas relevant for memory suggests enhanced reactivation of old fear memory trace in women. Sex differences in "gut memories" could play a role in the female preponderance of chronic abdominal pain. SN - 1095-9564 UR - https://www.unboundmedicine.com/medline/citation/24398396/Towards_understanding_sex_differences_in_visceral_pain:_enhanced_reactivation_of_classically_conditioned_fear_in_healthy_women_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1074-7427(13)00270-0 DB - PRIME DP - Unbound Medicine ER -