In the adult brain, space and orientation are represented by an elaborate hippocampal-parahippocampal circuit consisting of head-direction cells, place cells, and grid cells. We report that a rudimentary map of space is already present when 2 1/2-week-old rat pups explore an open environment outside the nest for the first time. Head-direction cells in the pre- and parasubiculum have adultlike properties from the beginning. Place and grid cells are also present but evolve more gradually. Grid cells show the slowest development. The gradual refinement of the spatial representation is accompanied by an increase in network synchrony among entorhinal stellate cells. The presence of adultlike directional signals at the onset of navigation raises the possibility that such signals are instrumental in setting up networks for place and grid representation.
Local space is represented by a number of functionally specific cell types, including place cells in the hippocampus and grid cells, head direction cells, and border cells in the medial entorhinal cortex (MEC). These cells form a functional map of external space already at the time when rat pups leave the nest for the first time in their life, at the age of 2.5 weeks. However, while place cells have adult-like firing fields from the outset, grid cells have irregular and variable fields until the fourth week, raising doubts about their contribution to place cell firing at young age. Recording in MEC of juvenile rats, we show that, unlike grid cells, border cells express adult-like firing fields from the first days of exposure to an open environment, at postnatal days 16-18. Thus, spatial signals from border cells may be sufficient to maintain spatially localized firing in juvenile hippocampal place cells.
SummaryMammalian navigation is thought to depend on an internal map of space consisting of functionally specialized cells in the hippocampus and the surrounding parahippocampal cortices [1–7]. Basic properties of this map are present when rat pups explore the world outside of their nest for the first time, around postnatal day 16–18 (P16–P18) [8–10]. One of the first functions to be expressed in navigating animals is the directional tuning of the head direction cells [8, 9]. To determine whether head direction tuning is expressed at even earlier ages, before the start of exploration, and to establish whether vision is necessary for the development of directional tuning, we recorded neural activity in pre- and parasubiculum, or medial entorhinal cortex, from P11 onward, 3–4 days before the eyelids unseal. Head direction cells were present from the first day of recording. Firing rates were lower than in adults, and preferred firing directions were less stable, drifting within trials and changing completely between trials. Yet the cells drifted coherently, i.e., relative firing directions were maintained from one trial to the next. Directional tuning stabilized shortly after eye opening. The data point to a hardwired attractor network for representation of head direction in which directional tuning develops before vision and visual input serves primarily to anchor firing direction to the external world.
SignificanceThe mammalian brain has neurons that specifically represent the animal’s location in the environment. Place cells in the hippocampus encode position, whereas grid cells in the medial entorhinal cortex, one synapse away, also express information about the distance and direction that the animal is moving. In this study, we show that, in 2.5–3-wk-old rat pups, place cells have firing fields whose positions depend on distance travelled, despite the immature state of grid fields at this age. The results suggest that place fields can be generated from self-motion–induced distance information in the absence of fully matured grid patterns.
Summary 23The sense of direction is a vital computation, whose neural basis is considered to be carried out 24 by head-direction cells. One way to estimate head-direction is by integrating head angular-25 velocity over time. However, this process results in error accumulation resembling a random 26 walk, proportional to √ , which constitutes a mark for a path integration process. In the present 27 study we analyzed previously recorded data to quantify the drift in head-direction cells of rat 28 pups before and after eye-opening. We found that in rat pups before eye-opening the drift 29 propagated as a random walk, while in rats after eye-opening the drift was lower. This suggests 30 that a path-integration process underlies the estimation of head-direction, such that before eye-
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