Brain responses to the vicarious facilitation of pain by facial expressions of pain and fear.

Abstract

Observing pain in others facilitates self-pain in the observer. Vicarious pain facilitation mechanisms are poorly understood. We scanned 21 subjects while they observed pain, fear and neutral dynamic facial expressions. In 33% of the trials, a noxious electrical stimulus was delivered. The nociceptive flexion reflex (NFR) and pain ratings were recorded. Both pain and fear expressions increased self-pain ratings (fear > pain) and the NFR amplitude. Enhanced response to self-pain following pain and fear observation involves brain regions including the insula (INS) (pain > fear in anterior part), amygdala, mid-cingulate cortex (MCC), paracentral lobule, precuneus, supplementary motor area and pre-central gyrus. These results are consistent with the motivational priming account where vicarious pain facilitation involves a global enhancement of pain-related responses by negatively valenced stimuli. However, a psychophysiological interaction analysis centered on the left INS revealed increased functional connectivity with the aMCC in response to the painful stimulus following pain observation compared to fear. The opposite connectivity pattern (fear > pain) was observed in the fusiform gyrus, cerebellum (I-IV), lingual gyrus and thalamus, suggesting that pain and fear expressions influence pain-evoked brain responses differentially. Distinctive connectivity patterns demonstrate a stronger effect of pain observation in the cingulo-insular network, which may reflect partly overlapping networks underlying the representation of pain in self and others.