How the Internally Organized Direction Sense Is Used to Navigate

Head-direction cells preferentially discharge when the head points in a particular azimuthal direction, are hypothesized to collectively function as a single neural system for a unitary direction sense, and are believed to be essential for navigating extra-personal space by functioning like a compass. We tested these ideas by recording medial entorhinal cortex (MEC) head-direction cells while rats navigated on a familiar, continuously rotating disk that dissociates the environment into two spatial frames: one stationary and one rotating. Head-direction cells degraded directional tuning referenced to either of the externally referenced spatial frames, but firing rates, sub-second cell-pair action potential discharge relationships, and internally referenced directional tuning were preserved. MEC head-direction cell ensemble discharge collectively generates a subjective, internally referenced unitary representation of direction that, unlike a compass, is inconsistently registered to external landmarks during navigation. These findings indicate that MEC-based directional information is subjectively anchored, potentially providing for navigation without a stable externally anchored direction sense. [Display omitted] •Compass-like MEC head-direction cell tuning can degrade during effective navigation•MEC head-direction cells encode a consistent, internally organized direction sense•The MEC-encoded direction sense inconsistently registers to environmental landmarks•MEC-based navigation operates like an etak (variably oriented) system rather than a GPS Park et al. show that medial entorhinal cortex head-direction cell discharge is internally organized but registers inconsistently and temporarily to external landmarks during navigation, indicating the navigation system operates unlike a GPS but like variably oriented etak systems without a global reference.