Abstract
Pain perception temporarily exaggerates abrupt thermal stimulus changes revealing a mechanism for nociceptive temporal contrast enhancement (TCE). Although the mechanism is unknown, a non-linear model with perceptual feedback accurately simulates the phenomenon. Here we test if a mechanism in the central nervous system underlies thermal TCE. Our model successfully predicted an optimal stimulus, incorporating a transient temperature offset (step-up/step-down), with maximal TCE, resulting in psychophysically verified large decrements in pain response (“offset-analgesia”; mean analgesia: 85%, n = 20 subjects). Next, this stimulus was delivered using two thermodes, one delivering the longer duration baseline temperature pulse and the other superimposing a short higher temperature pulse. The two stimuli were applied simultaneously either near or far on the same arm, or on opposite arms. Spatial separation across multiple peripheral receptive fields ensures the composite stimulus timecourse is first reconstituted in the central nervous system. Following ipsilateral stimulus cessation on the high temperature thermode, but before cessation of the low temperature stimulus properties of TCE were observed both for individual subjects and in group-mean responses. This demonstrates a central integration mechanism is sufficient to evoke painful thermal TCE, an essential step in transforming transient afferent nociceptive signals into a stable pain perception.
Highlights
Attention and behavioral response to important stimulus features is the culmination of a cascade of filtering and amplification mechanisms in the nervous system
Temporal contrast enhancement in pain has far mainly been explored in the context of “offset analgesia” and a single stimulus pattern
We formally generalize this process to an entire class of stimuli with a nonlinear recurrent feedback model of temporal integration, and identify an invariance relationship underlying responses to step-wise dynamic stimuli
Summary
Attention and behavioral response to important stimulus features is the culmination of a cascade of filtering and amplification mechanisms in the nervous system. Asymmetric spatial interactions have been observed between time varying painful stimuli and simultaneous but remote noxious stimulation[7]. This at least reveals events in the CNS can interfere with pain dynamics because peripheral nociceptive neurons have receptive fields on the order of centimeters and are unaffected by remote stimulus changes[20, 21]. Responses to step-wise noxious stimuli cannot be reduced to a linear combination, or superposition, of responses to constituent boxcar stimuli, so this TCE is a nonlinear response We leverage this property to probe for a central mechanism using psychophysics, theoretical modeling, and painful thermal stimuli. Nonlinear integration across peripheral receptive fields is sufficient to demonstrate a central mechanism for nociceptive TCE
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