Involvement of the lateral habenula in fear memory
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ORIGINAL ARTICLE
Involvement of the lateral habenula in fear memory Laura Durieux1 · Victor Mathis1,2 · Karine Herbeaux1 · Marc–Antoine Muller1 · Alexandra Barbelivien1 · Chantal Mathis1 · Rémy Schlichter3 · Sylvain Hugel3 · Monique Majchrzak1 · Lucas Lecourtier1 Received: 24 December 2019 / Accepted: 16 June 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract Increasing evidence points to the engagement of the lateral habenula (LHb) in the selection of appropriate behavioral responses in aversive situations. However, very few data have been gathered with respect to its role in fear memory formation, especially in learning paradigms in which brain areas involved in cognitive processes like the hippocampus (HPC) and the medial prefrontal cortex (mPFC) are required. A paradigm of this sort is trace fear conditioning, in which an aversive event is preceded by a discrete stimulus, generally a tone, but without the close temporal contiguity allowing for their association based on amygdala-dependent information processing. In a first experiment, we analyzed cellular activations (c–Fos expression) induced by trace fear conditioning in subregions of the habenular complex, HPC, mPFC and amygdala using a factorial analysis to unravel functional networks through correlational analysis of data. This analysis suggested that distinct LHb subregions engaged in different aspects of conditioning, e.g. associative processes and onset of fear responses. In a second experiment, we performed chemogenetic LHb inactivation during the conditioning phase of the trace fear conditioning paradigm and subsequently assessed contextual and tone fear memories. Whereas LHb inactivation did not modify rat’s behavior during conditioning, it induced contextual memory deficits and enhanced fear to the tone. These results demonstrate the involvement of the LHb in fear memory. They further suggest that the LHb is engaged in learning about threatening environments through the selection of relevant information predictive of a danger. Keywords Amygdala · Hippocampus · Prefrontal cortex · c-fos · Chemogenetic · Context
Introduction Laura Durieux, Victor Mathis, Sylvain Hugel, Monique Majchrzak and Lucas Lecourtier equally contributed to this study. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00429-020-02107-5) contains supplementary material, which is available to authorized users. * Monique Majchrzak [email protected] * Lucas Lecourtier [email protected] 1
Université de Strasbourg, Centre National de La Recherche Scientifique, Laboratoire de Neurosciences Cognitives Et Adaptatives (LNCA), UMR 7364, 12 rue Goethe, 67000 Strasbourg, France
2
Present Address: Department of Neuroscience, Icahn School of Medicine at Mount Sinai, NY 10029–6574, USA
3
Institut des Neurosciences Cellulaires et Intégratives (INCI), UPR 3212, CNRS, 8 Allée du Général Rouvillois, 67000 Strasbourg, France
The lateral habenula (LHb) plays a key role in the integration of basal gan
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