Vector production via mental navigation in the entorhinal cortex

A cognitive map is a suitably structured representation that enables an agent to perform novel computations using prior experience, for instance planning a new route in a familiar space1,2. Recent work in mammals has found direct evidence for such structured representations in the presence of exogenous sensory inputs in both spatial3,4 and non-spatial domains5–15. Here, we test a foundational postulate of the original cognitive map theory1,16 that cognitive maps are recruited endogenously during mental navigation without external input. We recorded from the entorhinal cortex of monkeys in a mental navigation task that required animals to use a joystick to produce one-dimensional vectors between pairs of visual landmarks without sensory feedback about the intermediate landmarks. Animals’ ability to perform the task and generalize to new pairs indicated that they relied on a structured representation of the landmarks. Task-modulated neurons exhibited periodicity and ramping that matched the temporal structure of the landmarks. Neuron pairs with high periodicity scores had invariant cross-correlation structure, a signature of grid cell continuous attractor states17– 19. A basic continuous attractor network model of path integration20 augmented with a Hebbian learning mechanism provided an explanation of how the system endogenously recalls landmarks. The model also made an unexpected prediction that endogenous landmarks transiently slow down path integration, reset the dynamics, and thereby, reduce variability. Remarkably, this prediction was borne out of a reanalysis of behavior. Together, our findings connect the structured activity patterns in the entorhinal cortex to the endogenous recruitment of a cognitive map during mental navigation.