Context-dependent modulation of hippocampal and cortical recruitment during remote spatial memory retrieval

Joëlle Lopez, Karin Herbeaux, Brigitte Cosquer, Michel Engeln, Christophe Muller, Christine Lazarus, Christian Kelche, Bruno Bontempi, Jean-Christophe Cassel, Anne Pereira de Vasconcelos
Hippocampus. 2011-05-03; 22(4): 827-841
DOI: 10.1002/hipo.20943

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Lopez J(1), Herbeaux K, Cosquer B, Engeln M, Muller C, Lazarus C, Kelche C, Bontempi B, Cassel JC, de Vasconcelos AP.

Author information:
(1)Laboratoire d’Imagerie et de Neurosciences Cognitives, UMR 7237 Université de
Strasbourg-CNRS, IFR 37 des Neurosciences, GDR CNRS 2905 Neuromem, 12 rue Goethe,
F-67000 Strasbourg, France.

According to systems consolidation, as hippocampal-dependent memories mature over
time, they become additionally (or exclusively) dependent on extra-hippocampal
structures. We assessed the recruitment of hippocampal and cortical structures on
remote memory retrieval in a performance-degradation resistant (PDR; no
performance degradation with time) versus performance-degradation prone (PDP;
performance degraded with time) context. Using a water-maze task in two contexts
with a hidden platform and three control conditions (home cage, visible platform
with or without access to distal cues), we compared neuronal activation (c-Fos
imaging) patterns in the dorsal hippocampus and the medial prefrontal cortex
(mPFC) after the retrieval of recent (5 days) versus remote (25 days) spatial
memory. In the PDR context, the hippocampus exhibited greater c-Fos protein
expression on remote than recent memory retrieval, be it in the visible or hidden
platform group. In the PDP context, hippocampal activation increased at the
remote time point and only in the hidden platform group. In the anterior
cingulate cortex, c-Fos expression was greater for remote than for recent memory
retrieval and only in the PDR context. The necessity of the mPFC for remote
memory retrieval in the PDR context was confirmed using region-specific lidocaine
inactivation, which had no impact on recent memory. Conversely, inactivation of
the dorsal hippocampus impaired both recent and remote memory in the PDR context,
and only recent memory in the PDP context, in which remote memory performance was
degraded. While confirming that neuronal circuits supporting spatial memory
consolidation are reorganized in a time-dependent manner, our findings further
indicate that mPFC and hippocampus recruitment (i) depends on the content and
perhaps the strength of the memory and (ii) may be influenced by the
environmental conditions (e.g., cue saliency, complexity) in which memories are
initially formed and subsequently recalled.

Copyright © 2011 Wiley Periodicals, Inc.


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