Successful spatial navigation and orientation are critical for survival. Lesions to a brain region called the retrosplenial cortex (RSC) dramatically impair spatial orientation abilities, but little is known about how the RSC is able to carry out these GPS-like functions. Here, we build towards a comprehensive cellular and circuit understanding of the RSC. We identify a uniquely small and excitable pyramidal neuron and show that it is the primary recipient of spatially-relevant inputs to the RSC, allowing this cell to simultaneously encode both head speed and direction. We also discover a uniquely fast brain rhythm in the RSC and show that this rhythm is controlled precisely by the speed of movement. Finally, we demonstrate how some of the critical building blocks of RSC function are impaired in a preclinical model of Alzheimer’s disease (AD), laying the foundation for understanding why the majority of persons with AD suffer from pronounced spatial disorientation.