Entorhinal cortex represents task-relevant remote locations independently of CA1.

Neurons can collectively represent the current sensory experience during exploration or remote experiences during immobility. Remote representations can reflect learned associations and support learning. Neurons in medial entorhinal cortex (MEC) represent the animal's current location during movement, but little is known about MEC representations during immobility. We recorded hundreds of neurons simultaneously in MEC and CA1 as mice learned to associate pairs of rewarded locations. During immobility, the MEC neural population frequently represented positions far from the animal's location ('nonlocal coding'). Cells with spatial firing fields at remote locations drove nonlocal coding, even as cells representing the current position remained active. While MEC nonlocal coding has been reported during sharp-wave ripples in CA1, we observed nonlocal coding more often outside of ripples and saw less CA1-MEC coordination during nonlocal coding. Further, nonlocal coding preferentially represented remote task-relevant locations at appropriate times. Together, this work suggests that MEC nonlocal coding could strengthen associations between locations independently from CA1.