Retrosplenial and postsubicular head direction cells compared during visual landmark discrimination

Abstract

Visual landmarks are used by head direction (HD) cells to establish and help update the animal’s representation of head direction, for use in orientation and navigation. Two cortical regions that are connected to primary visual areas, postsubiculum (PoS) and retrosplenial cortex (RSC), possess HD cells but it is unclear why the brain needs both regions – one possibility is that they differ in how they process visual landmarks. To investigate this possibility, we compared PoS and RSC HD cell activity from rats exploring an arena in which correct HD orientation required discrimination of two opposing landmarks having high, moderate or low discriminability. RSC HD cells had higher firing rates than PoS HD cells and slightly lower modulation by angular head velocity, and anticipated actual head direction by ~48 ms, indicating that RSC spiking leads PoS spiking. Otherwise, we saw no differences in landmark processing, in that HD cells in both regions showed equal responsiveness to and discrimination of the cues, with cells in both regions having unipolar directional tuning curves and discriminating the highly discriminable cues better than the others. There was a small spatial component to the signal in some cells, consistent with their role in interacting with the place cell navigation system, and there was also slight modulation by running speed. Neither region showed theta modulation of HD cell spiking. That the cells can immediately respond to subtle differences in spatial landmarks is consistent with rapid processing of visual snapshots or scenes; similarities in PoS and RSC responding may be due to either similar computations performed on the visual inputs, or to rapid sharing of information between the regions. More generally, this two-cue HD cell paradigm may be a useful method for testing rapid spontaneous visual discrimination capabilities in other experimental settings.