Abstract

The hippocampal formation contains several classes of neuron which respond to an animal’s position and orientation in space. Acting as an integrated circuit, these cell types (Place, Grid, Head Direction and Boundary cells) are thought to encode a neural map of the space through which the animal is moving. In order to understand when and how this neural representation of space is created during development, we recorded the activity of single neurons from awake and behaving pre-weanling rat pups, from postnatal day 12 (P12) onwards. We found that Head Direction cells emerge early in development (around P14 ), even before animals have begun to explore their environment. Grid cells emerge several days later, at around P20 , roughly the same age that hippocampus-dependent spatial learning is first observed. By contrast to the abrupt emergence of Head Direction and Grid cells, the Place cell network gradually matures between 2 and 6 weeks of age. However, examples of adult-like Place cell firing can be found even at P14 . We also investigated which inputs could support stable Place cell firing at these young ages. We found that Boundary cells exist from at least P17 onwards, and that at this age, the boundaries of the recording arena have an foundational role in stabilising the place cell representation of space.