What’s in the mirror? FMRI responses in the monkey action observation network while observing conspecific transitive and intransitive hand and tail actions.

Abstract

Observing others’ actions is an important aspect of social behavior, especially in primates. Observation of other individuals in action elicits neural responses in the so-called ‘Action Observation Network (AON)’, which includes occipito-temporal brain regions as well as parietal and premotor portions of the sensorimotor system, the latter typically involved in planning and execution of these actions. A dominant view suggests that the parie-to-frontal portion of the AON in monkeys responds in particular to observing goal-directed actions that are part of the monkey`s own motor repertoire. Contrary to this, much broader responses have been demonstrated in homologue regions of the human AON, including responses to both familiar and unfamiliar actions, transitive and intransitive actions, or even abstract sequences of events. Here we examined the effects of action transitivity and motor familiarity by measuring fMRI responses (Siemens 3 Tesla) in three adult rhesus monkeys while they observed an animated 3D monkey model (using open-source software Blender) performing either object-directed reach-and-grasp and reach-and-touch actions, or intransitive reach-only actions, executed with either the hand/forelimb or the tail. Both univariate whole-brain and region-of-interest (ROI) analyses in addition to ROI multivariate pattern analyses were performed. In line with previous electrophysiology and neuroimaging data, observing another individual performing a hand grasp yielded significant responses throughout the AON. Interestingly, also observing object touch or intransitive reach movements yielded robust responses throughout the AON, even when these actions were executed with a tail instead of a forelimb effector. Contrary to the suggestion that monkey sensorimotor regions only respond during observation of goal-directed motor actions which are part of the observer`s own motor repertoire, these results suggest that also intransitive and unfamiliar actions yield responses in visual and motor portions of the monkey AON, in line with human neuroimaging data and current predictive coding models of action observation.