Same Action, Different Meaning: Neural substrates of Semantic Goal Representation

Abstract

ABSTRACTAccurate control over everyday goal-directed actions is mediated by sensory-motor predictions of intended consequences and their comparison with actual outcomes. Such online comparisons of the expected and re-afferent, immediate, sensory feedback are conceptualized as internal forward models. Current predictive coding theories describing such models typically address the processing of immediate sensory-motor goals, yet voluntary actions are also oriented towards long-term conceptual goals and intentions, for which the sensory consequence is sometimes absent or cannot be fully predicted. Thus, the neural mechanisms underlying actions with distal conceptual goals is far from being clear. Specifically, it is still unknown whether sensory-motor circuits also encode information regarding the global meaning of the action, detached from the immediate, movement-related goal. Therefore, using fMRI and behavioral measures, we examined identical actions (either right or left-hand button presses) performed for two different semantic intentions (‘yes’/‘no’ response to questions regarding visual stimuli). Importantly, actions were devoid of differences in the immediate sensory outcome. Our findings revealed voxel patterns differentiating the two semantic goals in the frontoparietal cortex and visual pathways including the Lateral-occipital complex, in both hemispheres. Behavioral results suggest that the results cannot be explained by kinetic differences such as force. To the best of our knowledge, this is the first evidence showing that semantic meaning is embedded in the neural representation of actions independent of immediate sensory outcome and kinetic differences.Significance statementA standing question in neuroscience concerns the nature of neural circuits representing conceptual information. Previous studies indicate that regions traditionally associated with movement kinematics, also encode symbolic action categories regardless of their specific motor scheme. However, it is currently unclear whether these sensory-motor circuits also play a role in the representation of the intention, for which an action was initiated. Our results demonstrate that an action’s intention, such as its semantic goal, can be discriminated based on neural activity patterns in motor and sensory regions. Moreover, our findings suggest that semantic goals are embedded in sensorimotor regions in a hand-dependent manner.