Ontogeny of neural circuits underlying spatial memory in the rat

Abstract

Spatial memory is a well-characterized psychological function in both humans and rodents. The combined computations of a network of systems including place cells in the hippocampus, grid cells in the medial entorhinal cortex and head direction cells found in numerous structures in the brain have been suggested to form the neural instantiation of the cognitive map as first described by Tolman in 1948. However, while our understanding of the neural mechanisms underlying spatial representations in adults is relatively sophisticated, we know substantially less about how this network develops in young animals. In this article we briefly review studies examining the developmental timescale that these systems follow. Electrophysiological recordings from very young rats show that directional information is at adult levels at the outset of navigational experience. The systems supporting allocentric memory, however, take longer to mature. This is consistent with behavioral studies of young rats which show that spatial memory based on head direction develops very early but that allocentric spatial memory takes longer to mature. We go on to report new data demonstrating that memory for associations between objects and their spatial locations is slower to develop than memory for objects alone. This is again consistent with previous reports suggesting that adult like spatial representations have a protracted development in rats and also suggests that the systems involved in processing non-spatial stimuli come online earlier.

Keywords: entorhinal cortex; grid cell; head direction cell; hippocampus; memory and learning; place cell; postnatal development; spatial representation.

Figure 1

Spatial representations at the outset of navigational experience. (A) Head direction cells show adult like directional coding and stability at P15. (B) Grid cells show grid like characteristics in their rate maps (top row) and spatial autocorrelations (middle row) from P16 to 18 but the regularity and specificity of the grid increases with age. Examples of adult like place cells from P16 to 18 (bottom row). (C) Percentage of cells passing criterion for being place and grid cells through development. Note that the proportion of both place and grid cells that pass the criterion increases with age. Adapted from Langston et al. (2010).

Figure 2

Development of memory for objects and objects in location. (A) Object recognition protocol (top row) and associative spatial recognition protocol (bottom row). Both tasks consist of a sample phase where rats are presented with two objects to explore (left schematics) followed by a 2 min delay and a test phase (right schematics) where rats are given different combinations of objects to test memory for object or object in location. Arrows in test phase schematics represent the novel object or combination of object and location that we would expect the rats to preferentially explore. (B) Performance on the object recognition and associative spatial recognition tasks. P30 rats showed significantly greater preference for the novel object-location association than the P24 rats (p < 0.05) while the groups did not differ in standard object recognition performance. (C) Total exploration of the objects in the sample phase of the two tasks. Note no significant difference between the groups and the trend is toward P24 rats showing greater levels of exploration.