Highlights
- •Fear learning to a nonpainful visceral sensation was established.
- •Decision-making underlying intensity judgments of visceral sensations was modelled.
- •Fear learning induced a bias in the perceptual decision-making process.
- •Decision-making was biased towards perceiving visceral sensations as more intense.
Abstract
A growing body of research has identified fear of visceral sensations as a potential
mechanism in the development and maintenance of visceral pain disorders. However,
the extent to which such learned fear affects visceroception remains unclear. To address
this question, we used a differential fear conditioning paradigm with nonpainful esophageal
balloon distensions of 2 different intensities as conditioning stimuli (CSs). The
experiment comprised of preacquisition, acquisition, and postacquisition phases during
which participants categorized the CSs with respect to their intensity. The CS+ was
always followed by a painful electrical stimulus (unconditioned stimulus) during the
acquisition phase and in 60% of the trials during postacquisition. The second stimulus
(CS−) was never associated with pain. Analyses of galvanic skin and startle eyeblink
responses as physiological markers of successful conditioning showed increased fear
responses to the CS+ compared with the CS−, but only in the group with the low-intensity
stimulus as CS+. Computational modeling of response times and response accuracies
revealed that differential fear learning affected perceptual decision-making about
the intensities of visceral sensations such that sensations were more likely to be
categorized as more intense. These results suggest that associative learning might
indeed contribute to visceral hypersensitivity in functional gastrointestinal disorders.
Perspective
This study shows that associative fear learning biases intensity judgements of visceral
sensations toward perceiving such sensations as more intense. Learning-induced alterations
in visceroception might therefore contribute to the development or maintenance of
visceral pain.
Key words
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Article info
Publication history
Published online: May 19, 2017
Accepted:
April 23,
2017
Received in revised form:
April 5,
2017
Received:
December 23,
2016
Footnotes
L.V.O. and I.V.D. contributed equally to this work as senior authors.
J.Z. was supported by a Personal Doctoral Mandate grant of the KU Leuven Research Council, the Centre for Excellence of Generalization Research in Ill Health and Psychopathology (PF/10/005, KU Leuven), and the “Asthenes” long-term structural funding (METH/15/011) - Methusalem grant by the Flemish Government. K.W. was supported by a grant of the Medical Research Council, United Kingdom. J.W.S.V. was supported by an Odysseus grant provided by the Research Foundation, Flanders, Belgium. J.W.S.V. and L.V.O. are Research Professors of the KU Leuven Special Research Fund (“Bijzonder Onderzoeksfonds”). N.W. is supported by a research grant funded by the Research Foundation, Flanders, Belgium (G085013N). H.G.L. is supported by a postdoctoral fellowship of the KU Leuven Special Research Fund. V.J.M. was supported by the Oppenheimer Memorial Trust (South Africa) and is now supported by an Innovation Postdoctoral Fellowship from the South African National Research Foundation.
The authors have no conflicts of interest to declare.
Supplementary data accompanying this article are available online at www.jpain.org and www.sciencedirect.com.
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© 2017 Published by Elsevier Inc. on behalf of the American Pain Society
