From Anticipation to the Experience of Pain: The Importance of Visceral Versus Somatic Pain Modality in Neural and Behavioral Responses to Pain-Predictive Cues

Koenen, Laura Ricarda; Icenhour, Adriane; Forkmann, Katarina; Theysohn, Nina; Forsting, Michael; Bingel, Ulrike; Elsenbruch, Sigrid

doi:10.1097/psy.0000000000000612

Cited by 29 publications

(25 citation statements)

References 49 publications

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“…In healthy individuals, we recently observed pharmacologically increased cortisol levels to induce a reduction in visceral pain thresholds and to affect the formation of pain-related emotional memories (8). Importantly, these effects appeared to be specific to the visceral domain and were not observed for somatic stimuli of identical intensities, in line with prior research on distinct mechanisms underlying the processing of visceral and somatic pain (39)(40)(41)(42), and suggesting that visceroception might be particularly vulnerable to stress and stress mediators. Our findings expand this evidence to the dimension of chronic stress, with putative clinical implications for vulnerability and resilience in health and in disorders of gut-brain communication.…”

Section: Discussionsupporting

confidence: 79%

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: 79%

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%

“…Participants were prompted to indicate how they perceived each of the visual cues by presenting a digitized vertical 200 mm scale with end points labeled "very unpleasant" and "very pleasant, " indicating "neutral" in the middle of the scale. These values were then transformed into a scale with end points −100 indicating "very pleasant, " 100 indicating "very unpleasant" and "neutral" at 0 as previously accomplished in all of our prior conditioning work with this visceral pain model (13,(19)(20)(21). After conditioning, contingency awareness was assessed with ratings on how often each of the visual cues was followed by a rectal distension with corresponding scale end points labeled "never" (0%) and "always" (100%).…”

Section: Behavioral Measures Of Emotional Learning and Contingency Awmentioning

confidence: 99%

“…Visceral pain is of high clinical relevance, specifically in conditions of the gut-brain axis like irritable bowel syndrome (IBS). Compared to other types of exteroceptive pain, visceral pain is considered to be characterized by a unique biological salience, as supported by greater visceral pain-related fear and enhanced pain-related learning (12,13), making this a suitable preclinical model to study pain-related attentional biases. While numerous studies addressed attentional biases toward threat only, safety cues signaling the absence of an aversive event were also found to induce attentional biases (14) and are prioritized under threatening conditions (15).…”

Section: Introductionmentioning

confidence: 99%

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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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“…To ensure the presentation of visual stimuli at the plateau of the pain stimuli, image presentation started with an individual delay after the onset of pain stimulation. 23…”

Section: Pain Stimulationmentioning

confidence: 99%

Does pain modality play a role in the interruptive function of acute visceral compared with somatic pain?

Kleine-Borgmann

Schmidt

Scharmach³

et al. 2021

Pain

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Acute pain captures attentional resources and interferes with ongoing cognitive processes, including memory encoding. Despite broad clinical implications of this interruptive function of pain for the pathophysiology and treatment of chronic pain conditions, existing knowledge exclusively relies on studies using somatic pain models. Visceral pain is highly prevalent and seems to be more salient and threatening, suggesting that the interruptive function of pain may be higher in acute visceral compared with somatic pain. Implementing rectal distensions as a clinically relevant experimental model of visceral pain along with thermal cutaneous pain for the somatic modality, we herein examined the impact of pain modality on visual processing and memory performance in a visual encoding and recognition task and explored the modulatory role of pain-related fear and expectation in 30 healthy participants. Despite careful and dynamically adjusted matching of stimulus intensities to perceived pain unpleasantness over the course of trials, we observed greater impairment of cognition performance for the visceral modality with a medium effect size. Task performance was not modulated by expectations or by pain-related fear. Hence, even at matched unpleasantness levels, acute visceral pain is capable of interfering with memory encoding, and this impact seems to be relatively independent of pain-related cognitions or emotions, at least in healthy individuals. These results likely underestimate the detrimental effect of chronic pain on cognitive performance, which may be particularly pronounced in acute and chronic visceral pain.

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From Anticipation to the Experience of Pain: The Importance of Visceral Versus Somatic Pain Modality in Neural and Behavioral Responses to Pain-Predictive Cues

Cited by 29 publications

References 49 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

Does pain modality play a role in the interruptive function of acute visceral compared with somatic pain?

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