The role of environmental boundaries in the ontogeny of the hippocampal neural code for space
2013
The hippocampal formation (HF) contains neurons whose firing represents a code for the position and orientation of an animal in space, across the vertebrate group. We studied the ontogeny of such spatially-tuned firing in the rat HF, investigating how and when sensory inputs are combined in order to construct a neural code for space during development. During the first 2-4 weeks of post-natal life, rats progressively begin to walk, explore their environment, and display learning in tests of spatial memory. Concurrently, spatially-tuned cell types emerge in the HF; first Head Direction cells at postnatal day 14 (P14), then Place cells, which gradually mature between P14 and P45, and finally Grid cells, which emerge from P20 onwards. In this study, we investigated the developmental time-course of another class of spatially-tuned cell, Boundary Vector Cells (BVCs), and what functional role they might play in development. BVCs are found in the subiculum of the HF, and encode proximity to the boundaries of an animal’s environment. We found subiculum neurons which fired selectively in response to the walls of the recording arena from P17 onwards. We tested whether the firing of such cells generalises to all boundaries to movement by; 1) introducing a barrier into the centre of the recording arena, 2) placing the animal in a completely novel recording arena and 3) removing the walls of the familiar recording arena, leaving the rat on an open platform. From P17 onwards, we found subiculum neurons which continued to respond to boundaries to movement in all three of these conditions. Finally, we asked what functional role BVCs could serve, particularly in relation to developing Place cells. We found that there was a striking correlation between the distance of a Place cell’s field from the closest wall, and the within- and across-trial spatial stability of its place field, in the youngest rat pups (P14 – P21). However, this correlation was absent in both adults and post-weanling rats (P22-P30). Boundaries to movement may therefore exert a significant influence on the developing hippocampus, acting to stabilise Place cell firing at the earliest stages of development.
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