Intracranial human recordings reveal intensity coding for the pain of others in the insula

Abstract

Based on neuroimaging data, the insula is considered important for people to empathize with the pain of others, whether that pain is perceived through facial expressions or the sight of limbs in painful situations. Here we present the first report of intracranial electroencephalographic (iEEG) recordings from the insulae collected while 7 presurgical epilepsy patients rated the intensity of a womans painful experiences viewed in movies. In two separate conditions, pain was deduced from seeing facial expressions or a hand being slapped by a belt. We found that broadband activity in the 20-190 Hz range correlated with the trial-by-trial perceived intensity in the insula for both types of stimuli. Using microwires at the tip of a selection of the electrodes, we additionally isolated 8 insular neurons with spiking that correlated with perceived intensity. Within the insula, we found a patchwork of locations with differing selectivities within our stimulus set, some representing intensity only for facial expressions, others only for the hand being hit, and others for both. That we found some locations with intensity coding only for faces, and others only for hand across simultaneously recorded locations suggests that insular activity while witnessing the pain of others cannot be entirely reduced to a univariate salience representation. Psychophysics and the temporal properties of our signals indicate that the timing of responses encoding intensity for the sight of the hand being hit are best explained by kinematic information; the timing of those encoding intensity for facial expressions are best explained by shape information in the face. In particular, the furrowing of the eyebrows and the narrowing of the eyes of the protagonist in the movies suffice to predict both the rating of and the timing of the neuronal response to the facial expressions. Comparing the broadband activity in the iEEG signal with spiking activity and an fMRI experiment with similar stimuli revealed a consistent spatial organization for the representation of intensity from our hand stimuli, with stronger intensity representation more anteriorly and around neurons with intensity coding. In contrast, for the facial expressions, we found that the activity at the three levels of measurement do not coincide, suggesting a more disorganized representation. Together, our intracranial recordings indicate that the insula encodes, in a partially intermixed layout, both static and dynamic cues from different body parts that reflect the intensity of pain experienced by others.