Concurrent response and action effect representations across the somatomotor cortices during novel task preparation

Abstract

Instructions allow us to fulfill novel and complex tasks on the first try. This skill has been linked to preparatory brain signals that encode upcoming demands in advance, facilitating novel performance. To deepen insight into these processes, we aimed to explore whether instructions pre-activated task-relevant motoric and perceptual neural states. Critically, we addressed whether these representations anticipated activity patterns guiding overt sensorimotor processing, which could reflect that internally simulating the novel task facilitates the preparation. To do so, we collected functional magnetic resonance imaging data while participants encoded and implemented novel stimulus-response associations. Participants also completed localizer tasks designed to isolate the neural representations of the mappings-relevant motor responses, perceptual consequences, and stimulus categories. Using canonical template tracking, we identified whether and where these sensorimotor representations were pre-activated. We found that response-related templates were encoded in advance in regions linked with action control, entailing not only the instructed responses but also their action effects. This result was particularly robust in primary motor and somatosensory cortices. While, following our predictions, we found a systematic decrease in the irrelevant stimulus templates’ representational strength compared to the relevant ones, this difference was due to below-zero estimates linked to the irrelevant category activity patterns. Overall, our findings reflect that instruction processing relies on the sensorimotor cortices to anticipate motoric and kinesthetic representations of prospective action plans, suggesting the engagement of motor imagery during novel task preparation. More generally, they stress that the somatomotor system could participate with higher-level frontoparietal regions during anticipatory task control.Significance StatementBy using instructions, humans can successfully implement novel stimulus-response mapping on the first try. Here, we investigated whether this skill entailed anticipating the mappings-relevant motoric and perceptual neural states before task execution. Using tailored pattern analyses and localizer tasks, we isolated a series of task-relevant sensorimotor neural representations and addressed whether they were pre-activated during novel mapping preparation. We found widespread anticipation of the response-related activity patterns, which not only entailed the relevant motor responses but also their perceptual consequences. This finding was particularly robust in primary somatomotor areas. Overall, our results stress the contribution of lower-level cortices during instructed performance, suggesting that when no experience with a task is available, simulating the prospective sensorimotor processing may facilitate optimal preparation.