Recalibration of path integration in hippocampal place cells

Summary Path integration is an evolutionarily conserved navigation strategy in which an organism updates an internal estimate of its position relative to the external world by integrating over time a movement vector representing distance and direction traveled1-4. Accurate path integration requires a finely tuned gain factor that relates the animal’s self-movement to the updating of position on the internal “cognitive map,” with external landmarks necessary to correct positional error that eventually accumulates5,6. Path-integration-based models of hippocampal place cells and entorhinal grid cells treat the path integration gain as a constant6-11, but behavioral evidence in humans suggests that the gain is modifiable12. Here we show physiological evidence from hippocampal place cells that the path integration gain is indeed a highly plastic variable that can be altered by continuous conflict between self-motion cues and feedback from external landmarks. In a novel, augmented reality system, visual landmarks were moved in proportion to the animal’s movement on a circular track, creating continuous conflict with path integration. Sustained exposure to this cue conflict resulted in predictable and sustained recalibration of the path integration gain, as estimated from the place cells after the landmarks were extinguished. We propose that this rapid plasticity keeps the positional update in register with the animal's movement in the external world over behavioral timescales (mean 50 laps over 35 minutes). These results also demonstrate that visual landmarks not only provide a signal to correct cumulative error in the path integration system, as has been previously shown1,5,13-16, but also rapidly fine-tune the integration computation itself.