Dentate gyrus is necessary for disambiguating similar object-place representations

Abstract

Objects are often remembered with their locations, which is an important aspect of event memory. Despite the well-known involvement of the hippocampus in event memory, detailed intrahippocampal mechanisms are poorly understood. In particular, no experimental evidence has been provided in support of the role of the dentate gyrus (DG) in disambiguating such events, even though computational models suggest otherwise. In the current study, rats encountered multiple objects in different locations and were required to discriminate the object-place paired associates for reward. Specifically, two different objects appeared in one of two locations (arms in a radial maze) that were relatively close to each other. Different objects were rewarded depending on the arm in which the objects appeared. The rats with colchicine-based, dorsal DG (dDG) lesions showed severe and sustained impairment in disambiguating the objects compared with controls (Experiment 1). The dDG-lesioned rats were normal, however, in discriminating four different objects presented (Experiment 2) in the same locations as in Experiment 1. Finally, when the two different objects used in Experiment 1 were presented at two remote locations (Experiment 3) involving less overlap between arm-associated contextual cues, the dDG-lesioned animals showed initial deficits in discriminating the objects, but gradually relearned the task, in contrast to the sustained deficits observed in Experiment 1. These results collectively suggest that the DG is necessary when the similarity is maximal between object-place paired associates due to overlapping object and/or spatial information, whereas its role becomes minimal as the overlap in either object or spatial information decreases.