Cerebral regulation of facial expressions of pain

Abstract

Facial expression of affective states plays a key role in social interactions. Interestingly, however, individuals differ substantially in their level of expressiveness, ranging from high expressive to stoic individuals. Here, we investigate which brain mechanisms underlie the regulation of facial expressiveness to acute pain. Facial responses, pain ratings, and brain activity (BOLD-fMRI) evoked by noxious heat and warm (control) stimuli were recorded in 34 human volunteers with different degrees of facial expressiveness. Within-subject and between-subject variations in blood oxygenation level-dependent (BOLD) responses were examined specifically in relation to facial responses. Pain expression was inversely related to frontostriatal activity, consistent with a role in downregulating facial displays. More detailed analyses of the peak activity in medial prefrontal cortex revealed negative BOLD responses to thermal stimuli, an effect generally associated with the default mode network. Given that this negative BOLD response was weaker in low expressive individuals during pain, it could reflect stronger engagement in, or reduced disengagement from, self-reflective processes in stoic individuals. The occurrence of facial expressions during pain was coupled with stronger primary motor activity in the face area and-interestingly-in areas involved in pain processing. In conclusion, these results indicate that spontaneous pain expression reflects activity within nociceptive pathways while stoicism involves the active suppression of expression, a manifestation of learned display rules governing emotional communication and possibly related to an increased self-reflective or introspective focus.

Figure 1.

Study design and detailed description of the experimental protocol.

Figure 2.

Between-subject analyses—correlations between facial expressiveness and brain responses: facial expressiveness was positively correlated with stronger brain activation in M1 (face area) and in several pain-related areas (top). In contrast, the degree of facial expressiveness in response to painful heat was negatively correlated with activation in prefrontal areas and caudate nucleus (bottom). *Directed search threshold at T = 2.84 (p = 0.05). Bonferroni-corrected for 12 pain-related regions.

Figure 3.

Within-subject analyses—differences between painful events with and without facial expressions of pain. A, Stronger brain activation was found in M1 (face area) and in several pain-related areas in trials where individuals displayed spontaneous pain expression (left). In contrast, stronger activation was found in prefrontal areas and caudate nucleus when no expression was displayed (right). B, In facially non/low-expressive individuals, the display of intentionally communicated facial expressions of pain was associated with increased activity in M1 (left) and reduced activity in prefrontal cortices and in the caudate nucleus (right). *Directed search threshold at T = 2.84 (p = 0.05). Bonferroni-corrected for 12 pain-related regions.