Grid cells of animals raised in spherical environments

The entorhinal cortex is part of a brain circuit for dynamic mapping of the local environment. One key component of this circuit is the grid cell, whose multiple firing fields tessellate the environment in a periodic hexagonal manner. Studies in young rats have shown that grid cells appear during the third to fourth week of postnatal development, approximately one week after the animals leave the nest for the first time. It is currently not known if this late appearance of adult-like grid cells reflects the late maturation of certain components of the neural circuit, such as the inhibitory network of entorhinal layer II, or whether specific spatial experience is required for grid patterns to stabilize. We addressed this question by testing the impact of early spatial experience in rats. Long Evans rats were raised in a spherical environment from birth to adulthood. The spherical environment (70 cm or 1 m diameter) was designed to minimize any experience with stable peripheral boundaries. The sphere was made with a frosted 8 mm acrylic material to prevent the animals from experiencing spatial cues outside the sphere. The inside of the sphere contained only bedding material covering the bottom surface, a centrally suspended water bottle, and dispersed food pellets. Rats raised in the sphere were implanted with microdrives for subsequent recording of entorhinal activity. All animal handling, both before and after implantation, was performed in complete darkness with experimenters wearing night vision goggles. Grid cells were then recorded on successive trials in the home sphere in darkness. Once the electrodes reached layer II of the medial entorhinal cortex the animals were exposed for the first time to an environment outside the sphere - a 1 m square box presented in normal room light with a variety of proximal and distal cues. When possible, single cells were recorded over days to assess whether representations adapt with experience. Hexagonal grid firing was observed in the home sphere as well as the novel square environment. However, in the square arena, the grid cells of sphere-raised animals often deviated from a perfect hexagonal organization. This abnormality persisted across many hours of exposure to the square arena, with light and with room cues. Further experiments with animals raised in cubic environments, made in the same frosted material that prevents the experience of distal spatial cues, will determine (i) the extent to which these effects are stronger than those expected in normal animals in any novel environment and (ii) whether deprivation of distal cues during development can permanently affect the response properties of grid cells.