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WIREs Cogn Sci
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The development of spatial and memory circuits in the rat

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We provide a concise review of recent studies related to the development of neural circuits supporting spatial navigation and memory in the rat. We chart the relative timeline of the emergence of the four main classes of spatially tuned neurons within the hippocampus and related limbic areas: head direction cells emerge earliest (postnatal day 12, P12), before the eyes of the rats are even open, followed by place cells and boundary responsive cells; grid cells emerge last, around the age of weaning (P21). The rate of maturation is unique to each type of neuron, with the head direction and grid cells showing rapid developmental spurts, in contrast to place cells, which show a more gradual trend of maturation. Interestingly, the emergence of allocentric spatial abilities occurs only after the full complement of spatial neurons becomes functional at P20–21, whereas associative processing in the place cell network is evident from as early as P16. We also present evidence supporting the view that the sensory inputs, which are particularly salient to adult spatial networks, may not be essential for the immature spatial system. Crucially, visual information, although more salient than other sensory modalities for anchoring the adult head direction system, does not appear to be essential for setting up the immature head direction network. We conclude by highlighting an urgent need for new theoretical models that can account for the sequential emergence of spatial cells, as well as the lack of primacy of vision in the early organization of the head direction network. WIREs Cogn Sci 2017, 8:e1424. doi: 10.1002/wcs.1424

Postnatal developmental timeline of sensorimotor capacities, spatial behavior, and spatial cell activity in the rat. Each colored bar delineates the time course of emergence (unshaded) and maturation (slant‐shaded) for each modality, behavior, or cell type. Red dots mark the emergence of a particular phenomenon.
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Place cells in preweanling rats are already capable of associative processing of sensory information, before the emergence of allocentric spatial navigation (Reprinted with permission from Ref . Copyright 2016 Oxford University Press). (a) Place cells display remapping when animals are introduced into a novel environment at P18. Firing rate maps for three example place cells recorded at P18 are shown as pups explored a familiar (left) and a novel (right) environment, demonstrating remapping. Pictorial depictions show bird's eye views of experimental environments. In the novel environment, all intramaze cues change, and extramaze cues are obscured by a black curtain. Each row shows one place cell, and peak firing rates (in Hz) are shown in the top left corner of each rate map. (b) Mean (±SEM) across‐trial stability between two exposures to the familiar environment (Fam vs Fam) and between a familiar and novel environment (Fam vs Novel) for preweanling place cells (weaning takes place at P21 in the lab), demonstrating a near‐zero correlation of place cell firing fields across the two environments. (c) Place cells are already capable of pattern completion and separation by P16. Firing rate maps for example preweanling place cells recorded while the rat pup was exposed to a familiar environment and three manipulations using visually identical replicas of portions of the recording environment: replica walls (‘Change Walls’), replica floor (‘Change Floor’), and replica walls and floor (‘Change Floor + Walls’). The first two conditions produce no change to place cell maps, whereas changing both walls and floor leads to remapping. Each row shows one place cell, and peak firing rates (in Hz) are shown in the top left corner of each rate map. Example place cells were recorded at P17 (‘Change Walls’, ‘Change Floor’) and P16 (‘Change Walls + Floor’). (d) Place field stability in different environmental manipulations described in (c), relative to a familiar environment (Fam) measured by average spatial correlation (±SEM) for preweanling pups. A nonlinear pattern of change is observed, whereby replica ‘Walls’ or ‘Floor’ produce no reduction in stability relative to a familiar baseline (pattern completion), whereas replica ‘Walls + Floor’ produces strong remapping (pattern separation).
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Grid cells emerge abruptly from P20 to 21. (a) Firing rate maps and spatial auto‐correlograms are shown for individual cells recorded across two trials (Trials 1 and 2) from the mEC from P16 to P20–21, as well as in the adult rat. Numbers in top left corner of firing rate maps are peak firing rates (in Hz), and in the top right corner are gridness scores. (b) The percentage of mEC cells that qualify as grid cells in preweanling rats (P16–21, in red), postweanling rats (P22–30, in green), and adult rats (Ad, in blue). Dashed line indicates the 95% confidence level that more grid cells are found than those expected in spatially random firing Asterisks represent significant differences at the p < 0.05 level.
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Place cells mature slowly in the rat and are more stable near environmental boundaries before weaning (Reprinted with permission from Ref . Copyright 2015 Elsevier). (a) Place cells in young pups carry less spatial information and are less stable across trials than in the adult rat. Firing rate maps of place cells recorded from rat pups at postnatal days (P) 16, 22, and in the adult rat (Ad). Two 10‐min‐long trials are shown (Trials 1 and 2), separated by 10 min during which the rat rested in a separate holding platform. Numbers in top left corners of firing rate maps are peak firing rates (in Hz). (b) A subset of place cells displaying adult‐like intertrial stability and spatial information scores can be recorded in rat pups as early as P14. Firing rate maps of place cells recorded from rat pups at P14, P15, and P16. Two 10‐min‐long trials are shown (Trials 1 and 2), separated by 10 min during which the rat rested in a separate holding platform. (c–d) Stability of the place signal away from environmental boundaries improves significantly after weaning. (c) Mean across‐trial stability (±SEM) of place cells with firing fields in the edge (Ed) and center (Cn) zones of the recording environment before weaning (Pre), postweaning (Post), and in the adult rat (Ad). Weaning occurs at P21 in the lab. (d) Scatter plots of across‐trial stability versus distance of the firing field from the wall, before weaning (P16–17), after weaning (P22–23), and in the adult rat (Ad). Lines of best fit that are significant to the P < 0.05 level are shown as solid black lines, and the r 2 and P for regression are indicated above each plot. (e) Pictorial representation of the contribution of boundary responsive and grid cells to the accuracy of the place signal close to and away from environmental boundaries. The emergence of grid cells at P21 coincides with the stabilization of place fields away from the edges of the environment.
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Head direction cells are present before eye opening and mature rapidly with vision onset (Reprinted with permission from Ref . Copyright 2015 Elsevier). (a) Polar plots of head direction cells recorded from rat pups at postnatal days (P) 12, 15, 20, and in the adult rat (Ad). Days relative to eye opening day (E) are shown in parentheses (E0 is eye opening day). Two 5‐min‐long trials are shown (Trials 1 and 2), separated by 5 min during which the rat rested in a separate holding platform. Insets show polar plots for the first and second half of Trial 1. For each polar plot, peak firing rate (in Hz) is shown in the top left corner, and Rayleigh vector score (a measure of directional tuning) is shown in the top right corner. (b–c) Head direction cells are anchored to a prominent visual cue within 24 h of eye opening. (b) Diagram of the experimental set up showing rotation of the prominent visual cue (in yellow) by 180° from Trial A (baseline) to Trial B (rotated). (c) Polar plots for one head direction cell from the same animal responding to the rotation of the visual cue across two consecutive days, the day of eye opening (E0), and 1 day after eye opening (E1). Numbers in top left corner of polar plots are peak firing rates (in Hz) and in the top right corner are Rayleigh vector scores.
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