Ready, steady, go! Development of spatial representations in the rat
Abstract
In mice and men, the hippocampal region is the central brain network for declarative memory and dynamic
representation of location. Hippocampal place cells and entorhinal grid cells use head direction, border and
speed input to form an internal map of the local environment, and provides continuous updates of a rat's
position in relation to its movements in space. In particular, the crystalline readout of individual grid cells is
unique, with stable periodic firing fields that cover the available space with a metric grid. The vast majority
of knowledge about the architecture and function of the hippocampal region comes from experiments in
adult models, and currently little is known about the anatomical and functional development of these
circuits and cell types. In the work presented here, we study the development of anatomical connectivity
and functional maturation of circuits in the hippocampal region. Our results show that early development
in the region is precocious and largely independent of spatial learning. Grid cells, however, stand out in that
they rely on recent experience with vertical boundaries in order to stabilize an equidistant grid lattice at
adult ages, suggesting a highly plastic network.
In paper I we show that the first projections from hippocampal subiculum to entorhinal cortex (EC) are
already present and adult-like in their topography in the first postnatal week. Moreover, in the second
postnatal week the early projections mature and expand in line with the adult topography. This highly
organized development of connections between hippocampus and EC is strikingly different than what is
seen during development of connectivity in primary sensory cortices. Our results indicate that the
hippocampal-entorhinal system is in a ready-to-use state just before the onset of exploratory navigation in
rat pups.
In paper II we found functional head direction cells before eye-opening in the pre- and parasubiculum of
rat pups. Without visual inputs, the cells did not maintain a stable preferred head direction. However,
simultaneously recorded cells drifted coherently, similarly to what is seen during rotation experiments in
the adult head direction system. Within a few hours after eye-opening, we recorded stable head direction
cells in two-week old rat pups that displayed adult characteristics. In line with our findings in paper I, the
parahippocampal head direction cells are indeed ready to use before eyelids unseal in rat pups, and need
minimal visual inputs to stabilize.
Unlike the early adult-like representation of head-direction cells, it is already known that grid cells need the
first two weeks after eye-opening to mature. In paper III we show that grid cells are sensitive to the absence
of vertical boundaries for stable anchoring of the grid, in both young and adult rats. Our results indicate
that experience in itself is sufficient to change the properties of the grid network in varying ages.