Coregistration of heading and visual inputs in retrosplenial cortex

Spatial cognition depends on an accurate representation of orientation within an environment. Head direction cells in distributed brain regions receive a range of sensory inputs, including proprioceptive, vestibular, and somatosensory information, but visual input is particularly important for aligning their responses to environmental landmarks. To investigate how population-level heading responses are aligned to visual input, we recorded from the retrosplenial cortex (RSC) of head-fixed mice in a moving environment using two-photon calcium imaging. RSC receives strong inputs from both visual and spatial regions, and lesions result in drift of heading direction cell tuning away from environmental landmarks. First, we show that RSC neurons are tuned to the animal’s relative orientation in the environment, even in the absence of head movement, exhibiting the same functional properties as previously defined head-direction cells. Next, we imaged axonal terminals in RSC, revealing that RSC receives functionally distinct projections from visual and thalamic areas. The information carried by these projections combine in RSC to form functional subclasses of neurons, two of which faithfully mirror RSC inputs, representing visually-biased or heading-biased information. However, a newly discovered class coregisters these visual and thalamic signals, combining them into a novel response profile only found in RSC. Finally, decoding analyses reveal unique contributions to heading representations from each subclass of RSC neurons. Whereas heading-biased cells contribute in both light-on and light-off conditions, visually-biased cells drive high decoder performance in light-on conditions only. The final class of cells utilizes information from both sources, resulting in improved decoding in light-on conditions while retaining information in light-off conditions. Together, our results indicate a circuit in RSC that contributes to anchoring heading representations to environmental visual landmarks.