Memory of occasional events in rats: Individual episodic memory profiles, flexibility and neural substrate

A. Veyrac, M. Allerborn, A. Gros, F. Michon, L. Raguet, J. Kenney, F. Godinot, M. Thevenet, S. Garcia, B. Messaoudi, S. Laroche, N. Ravel
Journal of Neuroscience. 2015-05-13; 35(19): 7575-7586
DOI: 10.1523/JNEUROSCI.3941-14.2015

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Veyrac A(1), Allerborn M(2), Gros A(3), Michon F(2), Raguet L(2), Kenney J(2),Godinot F(2), Thevenet M(2), Garcia S(2), Messaoudi B(2), Laroche S(4), Ravel N(5).

Author information:
(1)Centre National de la Recherche Scientifique, Centre de Neurosciences
Paris-Sud, Université Paris-Sud, Unité Mixte de Recherche 8195, F-91405 Orsay,
France, Unité Mixte de Recherche 5292, Centre National de la Recherche
Scientifique, Institute national de la santé et de la recherche médicale U1028,
University Lyon 1, Lyon Neuroscience Research Center, F-69366 Lyon, France.
(2)Unité Mixte de Recherche 5292, Centre National de la Recherche Scientifique,
Institute national de la santé et de la recherche médicale U1028, University Lyon
1, Lyon Neuroscience Research Center, F-69366 Lyon, France.
(3)Centre National de la Recherche Scientifique, Centre de Neurosciences
Paris-Sud, Université Paris-Sud, Unité Mixte de Recherche 8195, F-91405 Orsay,
France.
(4)Centre National de la Recherche Scientifique, Centre de Neurosciences
Paris-Sud, Université Paris-Sud, Unité Mixte de Recherche 8195, F-91405 Orsay,
France, .
(5)Unité Mixte de Recherche 5292, Centre National de la Recherche Scientifique,
Institute national de la santé et de la recherche médicale U1028, University Lyon
1, Lyon Neuroscience Research Center, F-69366 Lyon, France
.

In search for the mechanisms underlying complex forms of human memory, such as
episodic recollection, a primary challenge is to develop adequate animal models
amenable to neurobiological investigation. Here, we proposed a novel framework
and paradigm that provides means to quantitatively evaluate the ability of rats
to form and recollect a combined knowledge of what happened, where it happened,
and when or in which context it happened (referred to as episodic-like memory)
after a few specific episodes in situations as close as possible to a paradigm we
recently developed to study episodic memory in humans. In this task, rats have to
remember two odor-drink associations (what happened) encountered in distinct
locations (where it happened) within two different multisensory enriched
environments (in which context/occasion it happened), each characterized by a
particular combination of odors and places. By analyzing licking behavior on each
drinking port, we characterized quantitatively individual recollection profiles
and showed that rats are able to incidentally form and recollect an accurate,
long-term integrated episodic-like memory that can last ≥ 24 d after limited
exposure to the episodes. Placing rats in a contextually challenging recollection
situation at recall reveals the ability for flexible use of episodic memory as
described in humans. We further report that reversible inactivation of the dorsal
hippocampus during recall disrupts the animal’s capacity to recollect the
complete episodic memory. Cellular imaging of c-Fos and Zif268 brain activation
reveals that episodic memory recollection recruits a specific, distributed
network of hippocampal-prefrontal cortex structures that correlates with the
accuracy of the integrated recollection performance.

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