Hippocampal representations of homing based on path integration

The ability to plan and execute a journey to a specific destination is essential for the survival of individuals of different species. Purposeful navigation can be achieved using landmark-based navigation and path integration. During path integration, the animal integrates self-motion information to estimate its location. Path integration is needed when external landmarks, such as visual landmarks, odour or auditory cues, are unavailable or when the animal visits unfamiliar environments. The study of the neuronal basis of path integration has been hampered by the lack of behavioural paradigm assessing path integration that allows simultaneous in vivo electrophysiological recordings in freely moving animals. Lesion studies have shown that the hippocampus and parahippocampal area are involved in path integration but the firing activity of the spatially selective cells, such as place cells, during path integration is unknown. Here, we developed a new behavioural paradigm (Automated Path Integration or AutoPI) to study homing behaviour based on path integration. In this task, a mouse finds a movable lever on the arena, presses it and returns to its home base to collect a food reward. Using the AutoPI task, we could record the firing pattern of the neurons in a large arena and investigate their spatial properties during homing behaviour. We used silicon probes to record the activity of hippocampal pyramidal cells when mice were running in AutoPI. By comparing the firing activity of neurons in the AutoPI task and during random foraging, we detected a complete reorganisation of hippocampal ensembles. We also found that several hippocampal pyramidal cells were firing when the animal was close to the lever (lever-anchored cells), independently of the lever's location on the arena. The spatial stability of lever-anchored cells was reduced during the trials with inaccurate homing. Moreover, the firing activity of lever-anchored cells also predicted the homing direction of the mice. These findings describe how hippocampal neurons with object-anchored firing fields contribute to homing behavior based on path integration