Behavioral responses to noxious stimuli shape the perception of pain

Abstract

Pain serves vital protective functions. To fulfill these functions, a noxious stimulus might induce a percept which, in turn, induces a behavioral response. Here, we investigated an alternative view in which behavioral responses do not exclusively depend on but themselves shape perception. We tested this hypothesis in an experiment in which healthy human subjects performed a reaction time task and provided perceptual ratings of noxious and tactile stimuli. A multi-level moderated mediation analysis revealed that behavioral responses are significantly involved in the translation of a stimulus into perception. This involvement was significantly stronger for noxious than for tactile stimuli. These findings show that the influence of behavioral responses on perception is particularly strong for pain which likely reflects the utmost relevance of behavioral responses to protect the body. These observations parallel recent concepts of emotions and entail implications for the understanding and treatment of pain.

Figure 1. Paradigm.

Pain and touch stimuli of varying intensity were applied to the right hand of healthy human subjects. Pain stimuli were brief cutaneous laser stimuli which selectively activate nociceptive afferents without activating tactile afferents. Touch stimuli were v.Frey-filaments applied by a computer-controlled device for standardized somatosensory stimulation. Reaction times were measured as button releases with the stimulated hand. Perceptual ratings were obtained on numerical rating scales from 0–100. ISI, inter-stimulus interval.

Figure 2. Perceptual ratings and reaction times to pain and touch stimuli.

Mean ratings and reaction times for pain and touch stimuli of low, medium and high intensities are shown. Error bars indicate the standard deviation of individual means, i.e., they reflect the variability across subjects. Ratings increased and reaction times decreased with increasing intensity of pain and touch stimuli. ms, milliseconds; NRS, numerical rating scale.

Figure 3. Moderated multi-level mediation analyses of the relationships between stimulus, behavior and perception.

Left, The perception-behavior model reflecting the traditional view of perception-behavior relationships (upper panel) and the behavior-perception model reflecting an extension of the traditional view of relationships (lower panel). Right, Results of the moderated multi-level mediation analyses for both models for pain and touch. All effects of both models and modalities were by themselves significant with the exception of the direct effect in the perception-behavior model for touch stimuli. Significant differences between modalities (pain vs. touch) are marked by asterisks and differences in thickness of arrow lines. In the perception-behavior model (upper panel), the direct effect of stimulus on behavior and the mediation effect of perception did not differ between modalities. In the behavior-perception model (lower panel), the mediation effect of behavior was significantly stronger for pain than for touch. In contrast, the direct effect was significantly stronger for touch than for pain. All effects are quantified in original units (milliseconds for behavior in the upper panel, ratings on the numerical rating scales for perception in the lower panel) so that coefficients reflect the estimated average effects of a one level stimulus intensity increase on the respective dependent variable. n.s., not significant; ***p < 0.001.

Figure 4. Replication of results in a control experiment.

Mediation effects, direct effects and the proportion of mediation effects to total effects and their 95% confidence intervals are shown for pain and touch in the perception-behavior (upper row) and the behavior-perception (lower row) model. Results from the main experiment (with block-wise presentation of pain and touch stimuli) are depicted using solid lines, results from the control experiment (with a mixed presentation of pain and touch stimuli within each block) using dashed lines. As in Fig. 3, all effects are depicted in original units and significant differences between modalities are marked. The control experiment fully replicated the pattern of results from the main experiment. ms, milliseconds; NRS, numerical rating scale; n.s., not significant; ***p < 0.001.