Predictable Context–Based Encoding of Observed Actions in Mirror Neurons of Macaque Premotor Area F5

Abstract

Mirror neurons have been believed to be crucial in processing information about others' behaviors, and the mainstream interpretation of their function is action understanding by mapping the observed action onto the motor repertoire of the subject, allowing the motor planning system of the observer to resonate. However, some recent studies using more sophisticated experiments have not been in line with it. The response selection hypothesis is a promising alternative theoretical framework to better interpret the properties of mirror neurons, but only several pieces of indirect evidence support it until now. In order to provide persuasive evidence, we trained two macaque monkeys using two paradigms (video-blocked paradigm and rule-blocked paradigm) in which the monkeys had to choose their action according to the demonstrator monkey’s transitive hand action in varying ways indicated by contextual information, and investigated whether the activity of F5 mirror neurons reflected the selection of a self-action based on the interpretation of another agent’s action. We recorded 859 neurons in the video-blocked paradigm and 288 neurons in the rule-blocked paradigm. Respectively, 500 (58.2%) and 228 (79.2%) of them were classified as mirror neurons and used in the analysis. We employed a novel analytical approach incorporating dimensionality reduction, allowing us to assign the information encoded by the population of F5 mirror neurons to the behavioral rule, observed action or the executed action. This approach enabled us to reveal the main drivers of neural activity and to trace their temporal dynamics, regardless of the presence of highly variable tuning at the level of individual neurons. The analysis showed that the influence of visual information on the activity of the F5 mirror neuron population is unexpectedly limited during the action observation. Instead, the dominant driver of neural activity during the action observation is the planning of the observer’s forthcoming action and the dominance gradually increased towards the execution phase. The gradual accumulation of action-related information according to earlier sensory and cognitive information is in line with that F5 matters for the context-dependent selection of actions.