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The Journal of Neuroscience, July 19, 2006, 26(29):7555-7564; doi:10.1523/JNEUROSCI.1068-06.2006

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Behavioral/Systems/Cognitive
Involvement of the Anterior Cingulate Cortex in the Expression of Remote Spatial Memory

Cátia M. Teixeira,^1,2 Stephen R. Pomedli,¹ Hamid R. Maei,^1,3 Nohjin Kee,¹ and Paul W. Frankland^1,3,4

¹Program in Neuroscience and Mental Health, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8, ²Graduate Program in Areas of Basic and Applied Biology, Universidade do Porto, 4050-345 Porto, Portugal, and ³Department of Physiology and ⁴Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada M5S1A8

Correspondence should be addressed to Paul W. Frankland, Program in Neuroscience and Mental Health, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8. Email: paul.frankland{at}sickkids.ca

Although the hippocampus plays a crucial role in the formation of spatial memories, as these memories mature they may become additionally (or even exclusively) dependent on extrahippocampal structures. However, the identity of these extrahippocampal structures that support remote spatial memory is currently not known. Using a Morris water-maze task, we show that the anterior cingulate cortex (ACC) plays a key role in the expression of remote spatial memories in mice. To first evaluate whether the ACC is activated after the recall of spatial memory, we examined the expression of the immediate early gene, c-fos, in the ACC. Fos expression was elevated after expression of a remote (1 month old), but not recent (1 d old), water-maze memory, suggesting that ACC plays an increasingly important role as a function of time. Consistent with the gene expression data, targeted pharmacological inactivation of the ACC with the sodium channel blocker lidocaine blocked expression of remote, but spared recent, spatial memory. In contrast, inactivation of the dorsal hippocampus disrupted expression of spatial memory, regardless of its age. We further showed that inactivation of the ACC blocked expression of remote spatial memory in two different mouse strains, after training with either a hidden or visible platform in a constant location, and using the AMPA receptor antagonist CNQX. Together, our data provide evidence that circuits supporting spatial memory are reorganized in a time-dependent manner, and establish that activity in neurons intrinsic to the ACC is critical for processing remote spatial memories.

Key words: hippocampus; spatial learning; Fos; lidocaine; CNQX; memory consolidation

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Received March 11, 2006; revised May 28, 2006; accepted May 31, 2006.

Correspondence should be addressed to Paul W. Frankland, Program in Neuroscience and Mental Health, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8. Email: paul.frankland{at}sickkids.ca

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