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

Abstract

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.

Involvement of the Anterior Cingulate Cortex in the Expression of Remote Spatial Memory

“…1m). Other types of control conditions have been used, including swimming controls (Gusev et al, 2005). However, whereas swimming controls equate swimming experience, reinforcement differs between groups and this may lead to differences in motivation and/or stress levels.…”

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

“…Within the context of this framework, there is evidence that parallels cellular and molecular consolidation processes necessary for gene transcription and protein synthesis after induction of LTP in this region. For example, increased expression of LTP-related immediate early genes (i.e., BDNF, zif268, c-FOS, and JUNB) in dorsal CA1 has been observed within 24 hr after the exposure to learning (Frey et al, 1991;Bertaina-Anglade et al, 2000;Gusev et al, 2005).…”

What Can Immediate-Early Gene Expression Tell Us about Spatial Memory Retrieval?

“…Recently, activation patterns of immediate-early genes have been used to shed light on this issue (Frankland and Bontempi, 2005). In a recent article in The Journal of Neuroscience, Gusev et al (2005) characterized the pattern of HC activation during the retrieval of recent or remote place memories acquired in the Morris water maze task using mRNA expression of the immediateearly gene Arc. The authors suggest that their results favor systems consolidation theory over MTT because they found a decrease in the magnitude and complexity of Arc expression in the HC as the memory aged.…”

“…The authors report a reduction in Arc mRNA in the HC during the retrieval of a remote memory for the platform compared with a recent memory [Gusev et al (2005), their Fig. 9 (http://www.…”

“…The authors conclude that this difference between subregions indicates a more persistent role for CA3 and dorsal HC neurons in the retrieval of water maze memory. By analyzing sections of the HC along the rostrocaudal axis, Gusev et al detected clusters of activation within subregions in dorsal and ventral HC [Gusev et al (2005), their Figs. 6 (http://www.jneurosci.org/cgi/ content/full/25/41/9384/FIG6), 7 (http:// www.jneurosci.org/cgi/content/full/25/ 41/9384/FIG7)].…”