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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, 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 retrosplenial cortex (RSC) of head-fixed mice in a moving environment using two-photon calcium imaging. We show that RSC neurons are tuned to the animal's relative orientation in the environment, even in the absence of head movement. Next, we found that RSC receives functionally distinct projections from visual and thalamic areas and contains several functional classes of neurons. While some functional classes mirror RSC inputs, a newly discovered class coregisters visual and thalamic signals. Finally, decoding analyses reveal unique contributions to heading from each class. Our results suggest an RSC circuit for anchoring heading representations to environmental visual landmarks., (© 2023. The Author(s).)

Perception of visual motion is important for a range of ethological behaviors in mammals. In primates, specific visual cortical regions are specialized for processing of coherent visual motion. However, whether mouse visual cortex has a similar organization remains unclear, despite powerful genetic tools available for measuring population neural activity. Here, we use widefield and 2-photon calcium imaging of transgenic mice to measure mesoscale and cellular responses to coherent motion. Imaging of primary visual cortex (V1) and higher visual areas (HVAs) during presentation of natural movies and random dot kinematograms (RDKs) reveals varied responsiveness to coherent motion, with stronger responses in dorsal stream areas compared to ventral stream areas. Moreover, there is considerable anisotropy within visual areas, such that neurons representing the lower visual field are more responsive to coherent motion. These results indicate that processing of visual motion in mouse cortex is distributed heterogeneously both across and within visual areas.