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The Journal of Neuroscience, January 21, 2009, 29(3):705-715; doi:10.1523/JNEUROSCI.3822-08.2009

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Behavioral/Systems/Cognitive
Mood Influences Supraspinal Pain Processing Separately from Attention

Chantal Villemure and M. Catherine Bushnell

Alan Edwards Centre for Research on Pain, McGill University, Montréal, Québec, Canada H3A 2B2

Correspondence should be addressed to Chantal Villemure, Alan Edwards Centre for Research on Pain, McGill University, Strathcona Anatomy and Dentistry Building, 3640 University Street, Room M-19, Montréal, Québec, Canada H3A 2B2. Email: chantal.villemure1{at}mcgill.ca

Studies show that inducing a positive mood or diverting attention from pain decreases pain perception. Nevertheless, induction manipulations, such as viewing interesting movies or performing mathematical tasks, often influence both emotional and attentional states. Imaging studies have examined the neural basis of psychological pain modulation, but none has explicitly separated the effects of emotion and attention. Using odors to modulate mood and shift attention from pain, we previously showed that the perceptual consequences of changing mood differed from those of altering attention, with mood primarily altering pain unpleasantness and attention preferentially altering pain intensity. These findings suggest that brain circuits involved in pain modulation provoked by mood or attention are partially separable. Here we used functional magnetic resonance imaging to directly compare the neurocircuitry involved in mood- and attention-related pain modulation. We manipulated independently mood state and attention direction, using tasks involving heat pain and pleasant and unpleasant odors. Pleasant odors, independent of attentional focus, induced positive mood changes and decreased pain unpleasantness and pain-related activity within the anterior cingulate (ACC), medial thalamus, and primary and secondary somatosensory cortices. The effects of attentional state were less robust, with only the activity in anterior insular cortex (aIC) showing possible attentional modulation. Lateral inferior frontal cortex [LinfF; Brodmann's area (BA) 45/47] activity correlated with mood-related modulation, whereas superior posterior parietal (SPP; BA7) and entorhinal activity correlated with attention-related modulation. ACC activity covaried with LinfF and periacqueductal gray activity, whereas aIC activity covaried with SPP activity. These findings suggest that separate neuromodulatory circuits underlie emotional and attentional modulation of pain.

Key words: pain; fMRI; attention; emotion; odor; heat

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Received Aug. 12, 2008; revised Dec. 1, 2008; accepted Dec. 4, 2008.

Correspondence should be addressed to Chantal Villemure, Alan Edwards Centre for Research on Pain, McGill University, Strathcona Anatomy and Dentistry Building, 3640 University Street, Room M-19, Montréal, Québec, Canada H3A 2B2. Email: chantal.villemure1{at}mcgill.ca

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