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The Journal of Neuroscience, April 19, 2006, 26(16):4437-4443; doi:10.1523/JNEUROSCI.4463-05.2006

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Behavioral/Systems/Cognitive
Isolating the Modulatory Effect of Expectation on Pain Transmission: A Functional Magnetic Resonance Imaging Study

John R. Keltner,¹ Ansgar Furst,² Catherine Fan,² Rick Redfern,² Ben Inglis,² and Howard L. Fields³

¹Pain Management Center, Department of Anesthesia and Perioperative Care, University of California San Francisco, San Francisco, California 94143, ²Henry H. Wheeler, Jr. Brain Imaging Center, Helen Wills Neuroscience Institute, University of California Berkeley, Berkeley, California 94608, and ³Wheeler Center for the Neurobiology of Addiction, Department of Neurology, University of California San Francisco, Emeryville, California 94608

Correspondence should be addressed to Dr. Howard L. Fields, Wheeler Center for the Neurobiology of Addiction, University of California San Francisco, 5858 Horton Street, Suite 200, Emeryville, CA 94608. Email: hlf{at}phy.ucsf.edu

We use a novel balanced experimental design to specifically investigate brain mechanisms underlying the modulating effect of expected pain intensity on afferent nociceptive processing and pain perception. We used two visual cues, each conditioned to one of two noxious thermal stimuli [48°C (high) or 47°C (low)]. The visual cues were presented just before and during application of the noxious thermal stimulus. Subjects reported significantly higher pain when the noxious stimulus was preceded by the high-intensity visual cue. To control for expectancy effects, for one-half of the runs, the noxious thermal stimuli were accompanied by the cue conditioned to the other stimulus. Comparing functional magnetic resonance imaging blood oxygenation level-dependent activations produced by the high and low thermal stimulus intensities presented with the high-intensity visual cue showed significant activations in nociceptive regions of the thalamus, second somatosensory cortex, and insular cortex. To isolate the effect of expectancy, we compared activations produced by the two visual cues presented with the high-intensity noxious thermal stimulus; this showed significant differences in the ipsilateral caudal anterior cingulate cortex, the head of the caudate, cerebellum, and the contralateral nucleus cuneiformis (nCF). We propose that pain intensity expectancy modulates activations produced by noxious stimuli through a distinct modulatory network that converges with afferent nociceptive input in the nCF.

Key words: pain modulation; brainstem; cingulate; cuneiformis; insula; sensory cortex

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Received Oct. 19, 2005; revised March 16, 2006; accepted March 18, 2006.

Correspondence should be addressed to Dr. Howard L. Fields, Wheeler Center for the Neurobiology of Addiction, University of California San Francisco, 5858 Horton Street, Suite 200, Emeryville, CA 94608. Email: hlf{at}phy.ucsf.edu

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