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Functional inactivation techniques enable studying the hippocampal involvement in each phase of spatial memory formation in the rat. In this study, we applied tetrodotoxin unilaterally or bilaterally into the dorsal hippocampus to evaluate the role of this brain structure in retrieval of memories acquired 28 days before in the Morris water maze. We combined hippocampal inactivation with the assessment of brain metabolism using cytochrome oxidase histochemistry. Several brain regions were considered, including the hippocampus and other related structures. Results showed that both unilateral and bilateral hippocampal inactivation impaired spatial memory retrieval. Hence, whereas subjects with bilateral hippocampal inactivation showed a circular swim pattern at the side walls of the pool, unilateral inactivation favoured swimming in the quadrants adjacent to the target one. Analysis of cytochrome oxidase activity disclosed regional differences according to the degree of hippocampal functional blockade. In comparison to control group, animals with bilateral inactivation showed increased CO activity in CA1 and CA3 areas of the hippocampus during retrieval, while the activity of the dentate gyrus substantially decreased. However, unilateral inactivated animals showed decreased CO activity in Ammon's horn and the dentate gyrus. This study demonstrated that retrieval recruits differentially the hippocampal subregions and the balance between them is altered with hippocampal functional lesions.

During extinction learning (EL), an individual learns that a previously learned behavior no longer fulfills its original purpose, or is no longer relevant. Recent studies have contradicted earlier theories that EL comprises forgetting, or the inhibition of the previously learned behavior, and indicate that EL comprises new associative learning. This suggests that the hippocampus is involved in this process. Empirical evidence is lacking however. Here, we used fluorescence in situ hybridization of somatic immediate early gene (IEG) expression to scrutinize if the hippocampus processes EL. Rodents engaged in context-dependent EL and were also tested for renewal of (the original behavioral response to) a spatial appetitive task in a T-maze. Whereas distal and proximal CA1 subfields processed both EL and renewal, effects in the proximal CA1 were more robust consistent with a role of this subfield in processing context. The lower blade of the dentate gyrus (DG) and the proximal CA3 subfields were particularly involved in renewal. Responses in the distal and proximal CA3 subfields suggest that this hippocampal subregion may also contribute to the evaluation of the reward outcome. Taken together, our findings provide novel and direct evidence for the involvement of distinct hippocampal subfields in context-dependent EL and renewal.

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