Evaluation of abstract rule-based associations in the human premotor cortex during passive observation

Abstract

Decision-making often manifests in behavior, typically yielding overt motor actions. This complex process requires the registration of sensory information with one’s internal representation of the current context, before a categorical judgment of the most appropriate motor behavior can be issued. The construct concept of embodied decision-making encapsulates this sequence of complex processes, whereby behaviorally salient information from the environment is represented in an abstracted space of potential motor actions rather than only in an abstract cognitive “decision” space. Theoretical foundations and some empirical evidence account for support the involvement of premotor cortical circuits in embodied cognitive functions. Animal models show that premotor circuits participate in the registration and evaluation of actions performed by peers in social situations, that is, prior to controlling one’s voluntary movements guided by arbitrary stimulus-response rules. However, such evidence from human data is currently limited. Here we used time-resolved magnetoencephalography imaging to characterize activations of the premotor cortex as human participants observed arbitrary, non-biological visual stimuli that either respected or violated a simple stimulus-response association rule. The participants had learned this rule previously, either actively, by performing a motor task (active learning), or passively, by observing a computer perform the same task (passive learning). We discovered that the human premotor cortex is activated during the passive observation of the correct execution of a sequence of events according to a rule learned previously. Premotor activation also differs when the subjects observe incorrect stimulus sequences. These premotor effects are present even when the observed events are of a non-motor, abstract nature, and even when the stimulus-response association rule was learned via passive observations of a computer agent performing the task, without requiring overt motor actions from the human participant. We found evidence of these phenomena by tracking cortical beta-band signaling in temporal alignment with the observation of task events and behavior. We conclude that premotor cortical circuits that are typically engaged during voluntary motor behavior are also involved in the interpretation of events of a non-ecological, unfamiliar nature but related to a learned abstract rule. As such, the present study provides the first evidence of neurophysiological processes of embodied decision-making in human premotor circuits when the observed events do not involve motor actions of a third party.