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The encoding of spatial, temporal, and affective dimensions in the dentate gyrus of the hippocampus

Abstract

Memory of an event must fundamentally include not only the time and place of its occurrence but also a measure of its significance for an organism to maintain and update the most relevant information in its world. It must then follow that the brain structures necessary for learning provide a mechanism to account for these details that cumulatively compose complex memories. To investigate the degree to which the hippocampus accounts for spatial, temporal and affective dimensions in its activity at the single cell and local field potential levels, in vivo electrophysiological recordings were performed in the dentate gyrus of rats during experiments explicitly designed to examine encoding along temporal and affective dimensions. First, to test for the presence of time- dependent single cell activity in the dentate gyrus, rats were exposed to three distinct behavioral contexts presented either simultaneously or separated in time. In this experiment, single cell activity accounted for temporal segregation of contexts by demonstrating activity selective to a single context. In a subset of rats with reduced levels of hippocampal adult neurogenesis, temporally selective contextual encoding was reduced, suggesting that adult neurogenesis contributes to the encoding of temporal dimensions. In a second experiment designed to examine mechanisms by which affective associations are made in the hippocampus, local field potentials were acquired from the dentate gyrus during reinforcement learning. Robust decreases in the amplitude of theta frequency oscillations (4-12Hz) occurred concurrently with increases in the amplitude of beta frequency oscillations during time intervals key to associational learning. These changes in amplitude were observed only during learning epochs and in the presence of reinforcers, suggesting that these oscillatory changes are dedicated to facilitating the encoding of associations with an affective dimension. The results of these experiments further our understanding of how complex memories requiring associations across multiple dimensions are formed in the hippocampus

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