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The Journal of Neuroscience, June 24, 2009, 29(25):8206-8214; doi:10.1523/JNEUROSCI.0966-09.2009

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Behavioral/Systems/Cognitive
The Formation of Recent and Remote Memory Is Associated with Time-Dependent Formation of Dendritic Spines in the Hippocampus and Anterior Cingulate Cortex

Leonardo Restivo,^1,2 * Gisella Vetere,^1,2 * Bruno Bontempi,³ and Martine Ammassari-Teule^1,2

¹Istituto di Neuroscienze del Consiglio Nazionale delle Ricerche, and ²Istituto di Ricovero e Cura a Carattere Scientifico, Fondazione Santa Lucia, 00143 Rome, Italy, and ³Centre de Neurosciences Intégratives et Cognitives, CNRS UMR 5228, Université de Bordeaux 1 et 2, 33405 Talence, France

Correspondence should be addressed to Martine Ammassari-Teule, Istituto di Ricovero e Cura a Carattere Scientifico, Fondazione Santa Lucia, Istituto di Neuroscienze del Consiglio Nazionale delle Ricerche, Via del Fosso di Fiorano 64, 00143 Rome, Italy. Email: martine.teule{at}cnr.it

Although hippocampal–cortical interactions are crucial for the formation of enduring declarative memories, synaptic events that govern long-term memory storage remain mostly unclear. We present evidence that neuronal structural changes, i.e., dendritic spine growth, develop sequentially in the hippocampus and anterior cingulate cortex (aCC) during the formation of recent and remote contextual fear memory. We found that mice placed in a conditioning chamber for one 7 min conditioning session and exposed to five footshocks (duration, 2 s; intensity, 0.7 mA; interstimulus interval, 60 s) delivered through the grid floor exhibited robust fear response when returned to the experimental context 24 h or 36 d after the conditioning. We then observed that their fear response at the recent, but not the remote, time point was associated with an increase in spine density on hippocampal neurons, whereas an inverse temporal pattern of spine density changes occurred on aCC neurons. At each time point, hippocampal or aCC structural alterations were achieved even in the absence of recent or remote memory tests, thus suggesting that they were not driven by retrieval processes. Furthermore, ibotenic lesions of the hippocampus impaired remote memory and prevented dendritic spine growth on aCC neurons when they were performed immediately after the conditioning, whereas they were ineffective when performed 24 d later. These findings reveal that gradual structural changes modifying connectivity in hippocampal–cortical networks underlie the formation and expression of remote memory, and that the hippocampus plays a crucial but time-limited role in driving structural plasticity in the cortex.

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Received Feb. 26, 2009; revised May 19, 2009; accepted May 20, 2009.

Correspondence should be addressed to Martine Ammassari-Teule, Istituto di Ricovero e Cura a Carattere Scientifico, Fondazione Santa Lucia, Istituto di Neuroscienze del Consiglio Nazionale delle Ricerche, Via del Fosso di Fiorano 64, 00143 Rome, Italy. Email: martine.teule{at}cnr.it

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