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From cue to meaning: Brain mechanisms supporting the construction of expectations of pain

Lobanov, Oleg V.a,b; Zeidan, Fadelb; McHaffie, John G.b; Kraft, Robert A.c; Coghill, Robert C.a,b,*

doi: 10.1016/j.pain.2013.09.014
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Summary Cues arising from different sensory modalities ultimately engage common brain mechanisms that reflect the meaning of the cue.

ABSTRACT The brain mechanisms by which sensory cues become transformed into expectations of impending events are a critical component of cognitive tuning of sensory processing. However, distinctions among the afferent processing of cue-related activity itself versus those mechanisms supporting the contextual meaning imparted to the cue remain limited. Do sensory cues with equal meaning engage similar patterns of brain activations even if they are delivered in separate modalities? To address this question, we used functional magnetic resonance imaging of an expectation paradigm in which cues were delivered with visual or innocuous thermal stimuli. Cues were designed to be highly meaningful because they predicted the delivery of high and low painful stimuli. As expected, the cues themselves activated unimodal sensory cortices. This cue modality-specific activation was transformed into a pattern of activity reflecting cue meaning. Cues signaling high pain produced greater activity in the left dorsolateral prefrontal cortex and anterior cingulate cortex. Such activity is consistent with the graded encoding of the magnitude of expected pain. In contrast, cues signaling low pain produced greater activity in the right intraparietal sulcus. This activation may reflect processes directing spatial attention to the stimulated body region in order to more accurately evaluate the relatively weak, low pain stimulus. Taken together, these findings indicate that cues arising from different sensory modalities ultimately engage common brain mechanisms that reflect the meaning of the cue. This meaning-related activity is presumably critical for preparing sensory systems to optimally process afferent information.

aNeuroscience Program, Wake Forest University School of Medicine, Winston-Salem, NC, USA

bDepartment of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC, USA

cDepartment of Biomedical Engineering, Wake Forest University School of Medicine, Winston-Salem, NC, USA

* Corresponding author. Address: Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, 1 Medical Center Boulevard, Winston-Salem, NC 27157-1010, USA. Tel.: +1 336 716 4284; fax: +1 336 716 4534.

E-mail address:rcoghill@wakehealth.edu

Article history:

Received 23 May 2013

Received in revised form 12 September 2013

Accepted 12 September 2013

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

© 2014 International Association for the Study of Pain
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