The reuniens and rhomboid nuclei are necessary for contextual fear memory persistence in rats

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ORIGINAL ARTICLE

The reuniens and rhomboid nuclei are necessary for contextual fear memory persistence in rats Etienne Quet1,2 · Monique Majchrzak1,2 · Brigitte Cosquer1,2 · Thomas Morvan1,2 · Mathieu Wolff3,4 · Jean‑Christophe Cassel1,2 · Anne Pereira de Vasconcelos1,2 · Aline Stéphan1,2  Received: 18 July 2019 / Accepted: 13 February 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Memory persistence refers to the process by which a temporary, labile memory is transformed into a stable and long-lasting state. This process involves a reorganization of brain networks at systems level, which requires functional interactions between the hippocampus (HP) and medial prefrontal cortex (mPFC). The reuniens (Re) and rhomboid (Rh) nuclei of the ventral midline thalamus are bidirectionally connected with both regions, and we previously demonstrated their crucial role in spatial memory persistence. We now investigated, in male rats, whether specific manipulations of ReRh activity also affected contextual and cued fear memory persistence. We showed that the permanent ReRh lesion impaired remote, but not recent contextual fear memory. Tone-cued recent and remote fear memory were spared by the lesion. In intact rats, acute chemogenetic ReRh inhibition conducted before recall of either recent or remote contextual fear memories produced no effect, indicating that the ReRh nuclei are not required for retrieval of such memories. This was also suggested by a functional cellular imaging approach, as retrieval did not alter c-fos expression in the ReRh. Collectively, these data are compatible with a role for the ReRh in ‘off-line’ consolidation of a contextual fear memory and support the crucial importance of ventral midline thalamic nuclei in systems consolidation of memories. Keywords  Fear memory · Hippocampus · Medial prefrontal cortex · Systems consolidation · Memory persistence · Ventral midline thalamus

Introduction The persistence of a memory requires that encoded information gradually stabilize, whereby becoming resistant to interference. Systems consolidation designates the progressive Anne Pereira De Vasconcelos and Aline Stéphan contributed equally to the work. * Aline Stéphan [email protected] 1



Laboratoire de Neurosciences Cognitives et Adaptatives, LNCA, UMR7364, CNRS, Université de Strasbourg, 67000 Strasbourg, France

2



Centre National de la Recherche Scientifique, LNCA UMR 7364, 67000 Strasbourg, France

3

Centre National de la Recherche Scientifique, INCIA, Unité Mixte de Recherche 5287, Bordeaux, France

4

Université de Bordeaux, INCIA, Unité Mixte de Recherche 5287, Bordeaux, France



reorganization of the brain structures that support memory persistence (Squire and Alvarez 1995; Frankland and Bontempi 2005). According to the standard theory of systems consolidation (Marr 1971), the initial information encoded with a contribution of the neocortex is integrated by the hippocampus (HP). After learning, off-line hippocampo-cortical reactivations occurring during sleep a