The post-natal development of sensory integration in place cells of pre-weanling rats

‘Place cells’ are hippocampal pyramidal neurons which fire only when an animal visits a particular location in an environment ( ‘place fields’). The resulting neural representation of space in the hippocampus is thought to support spatial memory and navigation. The location-specific firing of place cells is supported by configurations of multi-modal sensory cues. In this study, we investigated when the configural integration of sensory information first emerges during the post-natal development of the hippocampus, by probing the response of place cells in pre-weanling rat pups to manipulations of sensory cues. We recorded place cells whilst rats aged between postnatal days 16 and 24 explored a familiar open field environment. A significant number of cells showed stable, spatially localised firing, even at the youngest ages. To determine which sensory inputs supported stable spatial firing, we manipulated sensory cues, by 1) switching off the lights, 2) replacing the floor with a visually identical replica, or 3) placing pups in a completely novel environment. Changing the floor did not decrease place field stability in young rats more than it did in adults, indicating that place cells in young animals are not simply driven by local olfactory cues. Likewise, removing visual sensory information did not disproportionately reduce place field stability in young rats. At all ages, exposure to an entirely novel environment caused ‘remapping’ (a new, unpredictable set of place field locations). The spatial stability of place fields strongly correlated with distance of the field from the walls of the recording arena, suggesting that environmental boundaries are strong determinants of spatial firing in pre-weanling pups. Our results are compatible with the view that the place responses recorded in very young pre-weanling pups already integrate multimodal cues, as in adults, suggesting that hippocampal spatial responses are inherently configural.