Learning by experience? Visceral pain‐related neural and behavioral responses in a classical conditioning paradigm

Icenhour, Adriane; Labrenz, Franziska; Theysohn, Nina; Forsting, Michael; Bingel, Ulrike; Elsenbruch, Sigrid

doi:10.1111/nmo.13026

Cited by 30 publications

(27 citation statements)

References 57 publications

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“…The role of reporting bias and its possible contribution to findings of visceral hypersensitivity in IBS has previously been elegantly demonstrated (23). Our results expand on these data using a somewhat simpler yet clinically-relevant method, following a line of research on memory processes in visceroception (8,(19)(20)(21)(22), with a particular focus on interoceptive hypervigilance. It is indeed intriguing to speculate that chronic stress may contribute to interoceptive hypervigilance, either indirectly involving a reporting bias or more directly by biasing specific memory processes, including immediate recall, toward more "negative" memories of symptoms.…”

Section: Discussionsupporting

confidence: 65%

“…Future studies should therefore test the hypothesis that altered visceroceptive recall may constitute a nocebo mechanism in the pathophysiology of altered gut-brain interactions. Support for this assumption is provided by experimental findings from the field of associative visceral pain-related conditioning (19,21,22), with documented alterations in pain-related learning and memory processes in patients with IBS (20,38). Stress and stress mediators might play a key role in these alterations, as evidenced by findings that antagonizing corticotropin releasing factor, one of the main signaling peptides of the HPA axis released in response to stress, normalized aberrant neural and psychophysiological correlates of abdominal pain-related learning and memory in women with IBS (38).…”

Section: Discussionmentioning

confidence: 96%

“…Moreover, subclinical gastrointestinal (GI) symptoms experienced during a 3 month period preceding study participation were measured using a standardized in-house questionnaire (24). As in our prior studies (19,21,24) a cut-off score of 11 was used as an indicator of a putative undiagnosed gastrointestinal condition, which led to exclusion from study participation. Only women using hormonal contraception were included and pregnancy was ruled out on the study day with a commercially available urinary test.…”

Section: Participantsmentioning

confidence: 99%

“…This was accomplished given evidence that retrospective overall symptom ratings may be more susceptible to psychological modulation, especially in patients with IBS (18). Given our interest in visceral pain-related memory effects (8,(19)(20)(21)(22), together with evidence supporting the role of reporting bias in IBS (23), we introduced a new "memory bias" measure. This measure was based on the difference between perceptual ratings of individual distensions and retrospective overall ratings, the former being presumably more reflective of sensory-discriminative facts of visceroception, the latter possibly more prone to psychological modulation, both with relevance to collective symptom reporting in experimental and clinical trials as well as clinical practice.…”

Section: Introductionmentioning

confidence: 99%

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The Role of Chronic Stress in Normal Visceroception: Insights From an Experimental Visceral Pain Study in Healthy Volunteers

et al. 2020

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Visceroception is a complex phenomenon comprising the sensation, interpretation, and integration of sensations along the gut-brain axis, including pain or defecatory urgency. Stress is considered a crucial risk factor for the development and maintenance of disorders of gut-brain signaling, which are characterized by altered visceroception. Although the broad role of stress and stress mediators in disturbed visceroception is widely acknowledged, the putative contribution of chronic stress to variations in normal visceroception remains incompletely understood. We aimed to elucidate the role of chronic stress in shaping different facets of visceroception. From a well-characterized, large sample of healthy men and women (N = 180, 50% female), volunteers presenting with low (n = 57) and elevated (n = 61) perceived chronic stress were identified based on the validated Trier Inventory for Chronic Stress (TICS). Visceral sensitivity together with perceived and recalled intensity and defecatory urgency induced by repeated rectal distensions was experimentally assessed, and compared between low and elevated stress groups. Subgroups were compared regarding state anxiety and salivary cortisol concentrations across experimental phases and with respect to psychological measures. Finally, in the full sample and in chronic stress subgroups, a recall bias in terms of a discrepancy between the perception of experimentally-induced symptoms and their recall was tested. Participants with elevated chronic stress presented with increased state anxiety and higher cortisol concentrations throughout the experimental phases compared to the group with low chronic stress. Group differences in visceral sensitivity were not evident. The elevated stress group perceived significantly higher urgency during the stimulation phase, and recalled substantially higher feelings of urgency induced by rectal distensions, while perceived and recalled intensity were comparable between groups. Volunteers with elevated stress exhibited a recall bias in terms of a higher recall relative to mean perception of urgency, whereas no such bias was observed for the intensity of experimental visceral stimulation. Our findings in healthy men and women provide first evidence that the troublesome symptom of urgency might be particularly modifiable by chronic stress and support the relevance of memory biases in visceroception. These results may help to disentangle the impact of chronic stress on altered visceroception in disturbances of gut-brain communication.

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Section: Discussionsupporting

confidence: 65%

Section: Discussionmentioning

confidence: 96%

Section: Participantsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Role of Chronic Stress in Normal Visceroception: Insights From an Experimental Visceral Pain Study in Healthy Volunteers

et al. 2020

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“…The aim of this study was to elucidate attentional biases induced by pain-related conditioning in healthy women and men. To this end, we implemented a visual dot-probe task before and after differential fear conditioning with visceral pain as highly salient and clinically relevant interoceptive US (12,13,63). Conditioning successfully induced emotional pain-related learning to threat and safety cues, as evidenced by differential changes in cue valence.…”

Section: Discussionmentioning

confidence: 99%

Sex Differences Linking Pain-Related Fear and Interoceptive Hypervigilance: Attentional Biases to Conditioned Threat and Safety Signals in a Visceral Pain Model

2020

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Although the broad role of fear and hypervigilance in conditions of the gut-brain axis like irritable bowel syndrome is supported by converging evidence, the underlying mechanisms remain incompletely understood. Even in healthy individuals, it remains unclear how pain-related fear may contribute to pain-related attentional biases for acute visceral pain. Building on our classical fear conditioning work in a clinically relevant model of visceral pain, we herein elucidated pain-related attentional biases shaped by associative learning in healthy women and men, aiming to elucidate possible sex differences and the role of psychological traits. To this end, we compared the impact of differentially conditioned pain-predictive cues on attentional biases in healthy women and men. Sixty-four volunteers accomplished a visual dot-probe task and subsequently underwent pain-related fear conditioning where one visual cue (CS + ) was contingently paired with a painful rectal distention (US) while another cue remained unpaired (CS − ). During the following test phase, the dot-probe task was repeated to investigate changes in attentional biases in response to differentially valenced cues. While pain-related learning was comparable between groups, men revealed more pronounced attentional engagement with the CS + and CS − whereas women demonstrated stronger difficulties to disengage from the CS + when presented with a neutral cue. However, when both CS + and CS − were presented together, women revealed stronger difficulties to disengage from the CS − . Regression analyses revealed an interaction of sex, with negative affect predicting stronger avoidance of the CS + and stronger difficulties to disengage attention from the CS − in men. These results provide first evidence that pain-related fear conditioning may induce attentional biases differentially in healthy women and men. Hence, sex differences may play a role in attentional mechanisms underlying hypervigilance, and may be modulated by psychological vulnerability factors relevant to chronic visceral pain.

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Koenen

Elsenbruch

2018

Schmerz

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Interoceptive visceral pain is perceived as more fear-inducing and unpleasant compared to cutaneous heat pain in healthy women even when stimuli are matched for perceived pain intensity. On a neural level, both pain stimuli induce comparable neural activation in areas related to processing of sensory-discriminative pain aspects. However, enhanced neural responses are observed in areas associated with salience processing and descending pain inhibition for the visceral pain modality, even when results are controlled for intra-individual differences in perceived pain intensity. Moreover, immanent fear of pain is suggested to play a distinctive role in perception of visceral pain.

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Learning by experience? Visceral pain‐related neural and behavioral responses in a classical conditioning paradigm

Cited by 30 publications

References 57 publications

The Role of Chronic Stress in Normal Visceroception: Insights From an Experimental Visceral Pain Study in Healthy Volunteers

The Role of Chronic Stress in Normal Visceroception: Insights From an Experimental Visceral Pain Study in Healthy Volunteers

Sex Differences Linking Pain-Related Fear and Interoceptive Hypervigilance: Attentional Biases to Conditioned Threat and Safety Signals in a Visceral Pain Model

Schmerz ist modalitätsspezifisch

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