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The Journal of Neuroscience, October 12, 2005, 25(41):9384-9397; doi:10.1523/JNEUROSCI.0832-05.2005

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Behavioral/Systems/Cognitive
Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Pavel A. Gusev,¹ Changhai Cui,¹ Daniel L. Alkon,¹ and Alexander N. Gubin²

¹Blanchette Rockefeller Neurosciences Institute, Rockville, Maryland 20850, and ²Food and Drug Administration, Laboratory of Developmental Biology, Bethesda, Maryland 20892

The understanding of the mechanisms of memory retrieval and its deficits, and the detection of memory underlying neuronal plasticity, is greatly impeded by a lack of precise knowledge of the brain circuitry that underlies the functions of memory. The specific roles of anatomically distinct hippocampal subdivisions in recent and long-term memory retention and recall are essentially unknown. To address these questions, we mapped the expression of Arc/Arg 3.1 mRNA, a neuronal activity marker, in memory retention at multiple rostrocaudal levels of the dentate gyrus, CA3, CA1, subiculum, and lateral and medial entorhinal cortices after a platform search in a water-maze spatial task at 24 h and 1 month compared with swim and naive controls. We found that the entorhinohippocampal neuronal activity underlying the recall of recent and remote spatial memory has an anatomically distributed and time-dependent organization throughout both the dorsal and ventral hippocampus that is subdivision specific. We found a dissociation in the activity of the entorhinal cortex, CA3, and CA1 over a period of memory consolidation. Although CA3, the dorsal hippocampus, and the entorhinal cortex demonstrated the most persistent learning-specific signal during both recent and long-term memory recall, CA1 and the ventral hippocampus displayed the most dramatic signal decline. We determined the coordinates of activity clusters in the hippocampal subdivisions during the platform search and their dynamics over time. Our mapping data suggest that although the level of corticohippocampal interaction is similar during the retrieval of recent and remote spatial memories, the mnemonic function of the hippocampus may have changed, and the activity underlying remote spatial memory could be anatomically segregated within hippocampal subdivisions in small segments.

Key words: memory; stress; consolidation; hippocampus; water maze; immediate-early gene; corticosterone

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Received March 2, 2005; revised August 18, 2005; accepted August 18, 2005.

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