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Neural circuitry of abdominal pain-related fear learning and reinstatement in irritable bowel syndrome.
Neurogastroenterol Motil. 2015 Jan; 27(1):114-27.NM

Abstract

BACKGROUND

Altered pain anticipation likely contributes to disturbed central pain processing in chronic pain conditions like irritable bowel syndrome (IBS), but the learning processes shaping the expectation of pain remain poorly understood. We assessed the neural circuitry mediating the formation, extinction, and reactivation of abdominal pain-related memories in IBS patients compared to healthy controls (HC) in a differential fear conditioning paradigm.

METHODS

During fear acquisition, predictive visual cues (CS(+)) were paired with rectal distensions (US), while control cues (CS(-)) were presented unpaired. During extinction, only CSs were presented. Subsequently, memory reactivation was assessed with a reinstatement procedure involving unexpected USs. Using functional magnetic resonance imaging, group differences in neural activation to CS(+) vs CS(-) were analyzed, along with skin conductance responses (SCR), CS valence, CS-US contingency, state anxiety, salivary cortisol, and alpha-amylase activity. The contribution of anxiety symptoms was addressed in covariance analyses.

KEY RESULTS

Fear acquisition was altered in IBS, as indicated by more accurate contingency awareness, greater CS-related valence change, and enhanced CS(+)-induced differential activation of prefrontal cortex and amygdala. IBS patients further revealed enhanced differential cingulate activation during extinction and greater differential hippocampal activation during reinstatement. Anxiety affected neural responses during memory formation and reinstatement.

CONCLUSIONS & INFERENCES

Abdominal pain-related fear learning and memory processes are altered in IBS, mediated by amygdala, cingulate cortex, prefrontal areas, and hippocampus. Enhanced reinstatement may contribute to hypervigilance and central pain amplification, especially in anxious patients. Preventing a 'relapse' of learned fear utilizing extinction-based interventions may be a promising treatment goal in IBS.

Authors+Show Affiliations

Institute of Medical Psychology & Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

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

Language

eng

PubMed ID

25557224

Citation

Icenhour, A, et al. "Neural Circuitry of Abdominal Pain-related Fear Learning and Reinstatement in Irritable Bowel Syndrome." Neurogastroenterology and Motility : the Official Journal of the European Gastrointestinal Motility Society, vol. 27, no. 1, 2015, pp. 114-27.
Icenhour A, Langhorst J, Benson S, et al. Neural circuitry of abdominal pain-related fear learning and reinstatement in irritable bowel syndrome. Neurogastroenterol Motil. 2015;27(1):114-27.
Icenhour, A., Langhorst, J., Benson, S., Schlamann, M., Hampel, S., Engler, H., Forsting, M., & Elsenbruch, S. (2015). Neural circuitry of abdominal pain-related fear learning and reinstatement in irritable bowel syndrome. Neurogastroenterology and Motility : the Official Journal of the European Gastrointestinal Motility Society, 27(1), 114-27. https://doi.org/10.1111/nmo.12489
Icenhour A, et al. Neural Circuitry of Abdominal Pain-related Fear Learning and Reinstatement in Irritable Bowel Syndrome. Neurogastroenterol Motil. 2015;27(1):114-27. PubMed PMID: 25557224.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Neural circuitry of abdominal pain-related fear learning and reinstatement in irritable bowel syndrome. AU - Icenhour,A, AU - Langhorst,J, AU - Benson,S, AU - Schlamann,M, AU - Hampel,S, AU - Engler,H, AU - Forsting,M, AU - Elsenbruch,S, PY - 2014/09/11/received PY - 2014/11/18/accepted PY - 2015/1/6/entrez PY - 2015/1/6/pubmed PY - 2015/8/28/medline KW - extinction KW - fear conditioning KW - irritable bowel syndrome KW - pain-related fear KW - reinstatement KW - visceral pain SP - 114 EP - 27 JF - Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society JO - Neurogastroenterol Motil VL - 27 IS - 1 N2 - BACKGROUND: Altered pain anticipation likely contributes to disturbed central pain processing in chronic pain conditions like irritable bowel syndrome (IBS), but the learning processes shaping the expectation of pain remain poorly understood. We assessed the neural circuitry mediating the formation, extinction, and reactivation of abdominal pain-related memories in IBS patients compared to healthy controls (HC) in a differential fear conditioning paradigm. METHODS: During fear acquisition, predictive visual cues (CS(+)) were paired with rectal distensions (US), while control cues (CS(-)) were presented unpaired. During extinction, only CSs were presented. Subsequently, memory reactivation was assessed with a reinstatement procedure involving unexpected USs. Using functional magnetic resonance imaging, group differences in neural activation to CS(+) vs CS(-) were analyzed, along with skin conductance responses (SCR), CS valence, CS-US contingency, state anxiety, salivary cortisol, and alpha-amylase activity. The contribution of anxiety symptoms was addressed in covariance analyses. KEY RESULTS: Fear acquisition was altered in IBS, as indicated by more accurate contingency awareness, greater CS-related valence change, and enhanced CS(+)-induced differential activation of prefrontal cortex and amygdala. IBS patients further revealed enhanced differential cingulate activation during extinction and greater differential hippocampal activation during reinstatement. Anxiety affected neural responses during memory formation and reinstatement. CONCLUSIONS & INFERENCES: Abdominal pain-related fear learning and memory processes are altered in IBS, mediated by amygdala, cingulate cortex, prefrontal areas, and hippocampus. Enhanced reinstatement may contribute to hypervigilance and central pain amplification, especially in anxious patients. Preventing a 'relapse' of learned fear utilizing extinction-based interventions may be a promising treatment goal in IBS. SN - 1365-2982 UR - https://www.unboundmedicine.com/medline/citation/25557224/Neural_circuitry_of_abdominal_pain_related_fear_learning_and_reinstatement_in_irritable_bowel_syndrome_ L2 - https://doi.org/10.1111/nmo.12489 DB - PRIME DP - Unbound Medicine ER -