Landmark-Based Updating of the Head Direction System by Retrosplenial Cortex: A Computational Model

Maintaining a sense of direction is fundamental to navigation, and is achieved in the brain by a network of head direction (HD) cells, which update their signal using stable environmental landmarks. How landmarks are detected and their stability determined is still unknown. Recently we reported a new class of cells (Jacob et al., 2017), the bidirectional cells, in a brain region called retrosplenial cortex (RSC) which relays environmental sensory information to the HD system. A subset of these cells, between-compartment (BC) cells, are directionally tuned (like ordinary HD cells) but follow environmental cues in preference to the global HD signal, resulting in opposing (i.e., bidirectional) tuning curves in opposed environments. Another subset, within-compartment (WC) cells, unexpectedly expressed bidirectional tuning curves in each one of the opposed compartments. Both BC and WC cells lost directional tuning in an open field, unlike HD cells. Two questions arise from this discovery: (i) how do these cells acquire their unusual response properties, and (ii) what are they for? We propose that bidirectional cells reflect a two-way interaction between local direction, as indicated by the visual environment, and global direction as signaled by the HD system. We suggest that BC cells receive strong inputs from visual cues, while WC cells additionally receive modifiable inputs from HD cells which, due to Hebbian coactivation of visual inputs plus two opposing sets of HD inputs, acquire the ability to fire in both directions. A neural network model instantiating this hypothesis is presented, which indeed forms both BC and WC bidirectional cells with properties similar to those seen experimentally. We then demonstrate how tuning specificity degrades when WC/BC cells are exposed to multiple directionalities, replicating the observed loss of WC and BC directional tuning in the open field. We suggest that the function of these neurons is to assess the stability of environmental landmarks, thereby determining their utility as reference points by which to set the HD sense of direction. This role could extend to the ability of the HD system to prefer distal over proximal landmarks, and to correct for parallax errors.