Ready, steady, go! Development of spatial representations in the rat
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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.