Diverse long-range projections convey position information to the retrosplenial cortex.
Neuronal signals encoding the animals position, originally discovered in the hippocampus, widely modulate neocortical processing. While it is assumed that these signals 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 navigation and memory. Using two-photon axonal imaging in head-fixed mice performing a spatial task, we performed a comprehensive functional characterization of long-range inputs to agranular RSC. Surprisingly, most long-range pathways convey position information, but with key differences. We found that axons from the secondary motor cortex transmit the most position information. By contrast, axons from the posterior parietal-anterior cingulate- and orbitofrontal cortex and thalamus convey substantially less position information. Axons from the primary- and secondary visual cortex make a negligible contribution. These data show that RSC is a node in a widely distributed ensemble of networks that share position information in a projection-specific manner.