Hippocampal-entorhinal cognitive maps and cortical motor system represent action plans and their outcomes

Abstract

Efficiently interacting with the environment requires weighing and selecting among multiple alternative actions based on their associated outcomes. However, the neural mechanisms underlying these processes are still debated. We showed that forming relations between arbitrary action-outcome associations involved building a cognitive map. Using a novel immersive virtual reality paradigm, participants learned 2D abstract motor action-outcome associations and later compared action combinations while their brain activity was monitored with fMRI. We observed a hexadirectional modulation of the activity in entorhinal cortex while participants compared different action plans. Furthermore, hippocampal activity scaled with the 2D similarity between outcomes of these action plans. Conversely, the supplementary motor area (SMA) represented individual actions, showing a stronger response to overlapping action plans. Crucially, the connectivity between hippocampus and SMA was modulated by the similarity between the action plans, suggesting their complementary roles in action evaluation. These findings provide evidence for the role of cognitive maps in action selection, challenging classical models of memory taxonomy and its neural bases.