Age-related changes in hippocampal map realignment

Abstract

The activity of hippocampal pyramidal cells (place cells) is correlated with the position of a rat in a given environment, suggesting that the rat hippocampus may contain a cognitive map of the environment. Internally-generated information about the motion of the rat may be the strongest initial determinant of place-cell firing. With experience in a given environment, cues and landmarks may gain control over place-cell firing, allowing the correction of errors or drift in the self-motion information. This 'binding' of cues to the hippocampal map may involve long-term potentiation (LTP). Because hippocampal LTP is impaired in aged rats, cues and landmarks should be poorly bound to the hippocampal map in aged rats. To test this prediction, aged and adult rats were trained to run back and forth on a linear track. The position of the start box was changed from trial to trial, so that self-motion information (i.e., the distance of the rat from the start box) and visual-cue information (the position of the rat in the room) were mismatched. In this situation, self-motion information controls place-cell firing during the initial portion of each journey. At some point in each journey, however, the hippocampal map realigns, so that place-cell firing is controlled by visual-cue information. If age-related LTP deficits impair the binding of cues to the hippocampal map, this realignment should be delayed in aged rats. As predicted, the realignment occurred nearer to the end of the track in the aged rats. Moreover, the delayed realignment was correlated with the rats' ability to find a hidden goal at a position relative to the visual cues. The results suggest that some of the spatial-learning deficits observed in aged rats may be due to impaired binding of cues to the hippocampal map. In addition, despite the fact that the animals in the present study had never been trained with a stable start box (the anchor point for self-motion information), place-cell firing was controlled by self-motion information for a large portion of each outbound journey. This result supports a strong initial role of self-motion information in determining the hippocampal representation of a rat's position.