Multiple long-range projections convey position information to the agranular retrosplenial cortex

Neuronal signals encoding the animal's position widely modulate neocortical processing. While these signals are assumed to depend on hippocampal output, their origin has not been investigated directly. Here, we asked which brain region sends position information to the retrosplenial cortex (RSC), a key circuit for memory and navigation. We comprehensively characterized the long-range inputs to agranular RSC using two-photon axonal imaging in head-fixed mice performing a spatial task in darkness. Surprisingly, most long-range pathways convey position information, but with notable differences. Axons from the secondary motor and posterior parietal cortex transmit the most position information. By contrast, axons from the anterior cingulate and orbitofrontal cortex and thalamus convey substantially less position information. Axons from the primary and secondary visual cortex contribute negligibly. This demonstrates that the hippocampus is not the only source of position information. Instead, the RSC is a hub in a distributed brain network that shares position information.