A crucial feature of socially adaptive behavior is the ability to recognize when our actions harm other individuals. Previous research demonstrates that dorsal mediofrontal cortex (dMFC) and anterior insula (AI) are involved in both action monitoring and empathy for pain. Here, we tested whether these regions could integrate monitoring of error agency with the representation of others' pain. While undergoing event-related fMRI, participants played a visual task in turns with a friend placed outside the scanner, who would receive painful stimulation in half of the error trials. Brain activity was enhanced in dMFC and AI for painful compared with nonpainful errors. Left AI and dorsolateral pFC also exhibited a significant interaction with agency and increased responses when painful errors were caused by oneself. We conclude that AI is crucial for integrating inferences about others' feeling states with information about action agency and outcome, thus generating an affective signal that may guide subsequent adjustment.

Embodied theories hold that understanding what another person is doing requires the observer to map that action directly onto his or her own motor representation and simulate it internally. The human motor system may, thus, be endowed with a “mirror matching” device through which the same motor representation is activated, when the subject is either the performer or the observer of another's action (“self-other shared representation”). It is suggested that understanding action verbs relies upon the same mechanism; this implies that motor responses to these words are automatic and independent of the subject of the verb. In the current study, participants were requested to read silently and decide on the syntactic subject of action and nonaction verbs, presented in first (1P) or third (3P) person, while TMS was applied to the left hand primary motor cortex (M1). TMS-induced motor-evoked potentials were recorded from hand muscles as a measure of cortico-spinal excitability. Motor-evoked potentials increased for 1P, but not for 3P, action verbs or 1P and 3P nonaction verbs. We provide novel demonstration that the motor simulation is triggered only when the conceptual representation of a word integrates the action with the self as the agent of that action. This questions the core principle of “mirror matching” and opens to alternative interpretations of the relationship between conceptual and sensorimotor processes.