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Modality-specific effects of aversive expectancy in the anterior insula and medial prefrontal cortex

Sharvit, Gila,b,c,*; Corradi-Dell'Acqua, Corradoa,b,d; Vuilleumier, Patrika,b

doi: 10.1097/j.pain.0000000000001237
Research Paper

Expectations modulate the subjective experience of pain by increasing sensitivity to nociceptive inputs, an effect mediated by brain regions such as the insula. However, it is still unknown whether the neural structures underlying pain expectancy hold sensory-specific information or, alternatively, code for modality-independent features (eg, unpleasantness), potentially common with other negative experiences. We used functional magnetic resonance imaging to investigate neural activity underlying the expectation of different, but comparably unpleasant, pain and disgust. We presented participants with visual cues predicting either a painful heat or disgusting odor, and assessed how they affected the subsequent subjective experience of stimuli from the same (within-modality) or opposite (cross-modal) modality. We found a reliable influence of expectancy on the subjective experience of stimuli whose modality matched that of the previous cue. At the brain level, this effect was mediated by the intermediate dysgranular section of the insula, whereas it was suppressed by more anterior agranular portions of the same region. Instead, no expectancy modulation was observed when the modality of the cue differed from that of the subsequent stimulus. Our data suggest that the insular cortex encodes prospective aversive events in terms of their modality-specific features, and whether they match with subsequent stimulations.

The right anterior insula codes prospective pain and disgust in terms of their modality-specific features.

aLaboratory for Neurology and Imaging of Cognition, Department of Neurosciences and Clinic of Neurology, University Medical Centre, Geneva, Switzerland

bSwiss Centre for Affective Sciences, University of Geneva, Geneva, Switzerland

cNeuroeconomics Laboratory at Haas School of Business, University of California, Berkeley, Berkeley, CA, United States

dDepartment of Psychology, FPSE, University of Geneva, Geneva, Switzerland

Corresponding author. Address: Neuroeconomics Laboratory at Haas School of Business, University of California, Berkeley, 2220 Piedmont Ave, Berkeley, CA 94720, United States. Tel.: +1 510 725 2592. E-mail address: sharvit@berkeley.edu (G. Sharvit).

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.painjournalonline.com).

C. Corradi-Dell'Acqua and P. Vuilleumier contributed equally to this work.

Received August 02, 2017

Received in revised form March 20, 2018

Accepted March 29, 2018

© 2018 International Association for the Study of Pain
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