Neural correlates of the prolonged salience of painful stimulation.
Pain is a unique class of sensory experience from the perspective of salience. Nonpainful somatosensory stimuli usually require behavioral relevance or voluntary attention to maintain salience. In contrast, painful stimuli tend to have sustained salience even without explicit behavioral relevance or voluntary attention. We have previously identified a frontal-parietal-cingulate network of regions responding transiently to nonpainful sensory events. This network is sensitive to the task relevance and novelty of sensory events and likely represents the salience of events in the sensory environment. Since pain can remain salient for a prolonged period, we hypothesized that this network should show transient responses to the onset or offset of a nonpainful stimulus, but sustained responses throughout the duration of a painful stimulus. To test this hypothesis, we used functional MRI to examine the response of these regions to sustained (60-s) periods of painful and nonpainful transcutaneous electrical nerve stimulation. As predicted, the temporoparietal, inferior frontal, and anterior cingulate cortex showed only transient responses to the onset or offset of nonpainful stimulation, but a sustained response throughout the duration of painful stimulation. These regions therefore show tonic responses to stimuli with tonic salience, supporting a general role for these areas in representing stimulus salience. The thalamus and putamen also responded tonically throughout painful but not nonpainful stimulation. Previous studies have implicated the basal ganglia in supporting voluntary sustained attention. Our findings suggest that the basal ganglia may play a more general role in supporting sustained salience, whether through voluntary or involuntary mechanisms.
Downar
Jonathan
J
Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada M5T 2S8.
Mikulis
David J
DJ
Davis
Karen D
KD
D000328:Adult; D001519:Behavior / Q000502:physiology; D004558:Electric Stimulation; D005260:Female; D005625:Frontal Lobe / Q000502:physiology; D006179:Gyrus Cinguli / Q000502:physiology; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009042:Motivation; D009415:Nerve Net / Q000502:physiology; D009420:Nervous System / Q000503:physiopathology*; D010146:Pain / Q000503:physiopathology*; D010147:Pain Measurement; D010296:Parietal Lobe / Q000502:physiology; D010775:Photic Stimulation; D012201:Reward; D004561:Transcutaneous Electric Nerve Stimulation