Distinct brain networks for remote episodic memory depending on content and emotional experience

• Published in: Progress in neurobiology 2023-04, Vol.223, p.102422-102422, Article 102422
• Main Authors: Auguste, Anne, Fourcaud-Trocmé, Nicolas, Meunier, David, Gros, Alexandra, Garcia, Samuel, Messaoudi, Belkacem, Thevenet, Marc, Ravel, Nadine, Veyrac, Alexandra
• Format: Article
• Language: English
• Subjects: Animals; Brain; Cognitive science; Emotional content; Emotions; Hippocampus; Humans; Individual mnemonic function; Life Sciences; Memory engrams; Memory, Episodic; Memory, Long-Term; Mental Recall; Neurons and Cognition; Neuroscience; Odors; Rats; Remote episodic memory; Systems consolidation
• ISSN: 0301-0082; 1873-5118
• DOI: 10.1016/j.pneurobio.2023.102422

Memories of life episodes are the heart of individual stories. However, modelling episodic memory is a major challenge in both humans and animals when considering all its characteristics. As a consequence, the mechanisms that underlie the storage of old nontraumatic episodic memories remain enigmatic. Here, using a new task in rodents that models human episodic memory including odour/place/context components and applying advances behavioural and computational analyses, we show that rats form and recollect integrated remote episodic memories of two occasionally encountered complex episodes occurring in their daily life. Similar to humans, the information content and accuracy of memories vary across individuals and depend on the emotional relationship with odours experienced during the very first episode. We used cellular brain imaging and functional connectivity analyses, to find out the engrams of remote episodic memories for the first time. Activated brain networks completely reflect the nature and content of episodic memories, with a larger cortico-hippocampal network when the recollection is complete and with an emotional brain network related to odours that is critical in maintaining accurate and vivid memories. The engrams of remote episodic memories remain highly dynamic since synaptic plasticity processes occur during recall related to memory updates and reinforcement. •Rats form and recollect remote memories of occasional episodes of life.•Remote episodic memory differs in its content and level of detail from one individual to another.•Integrity of remote episodic memory depends on emotional experiences with odours during episodes.•Engram reflects the content of remote episodic memories with a key role of the emotional brain.•Synaptic plasticity processes during recall reflect memory updating and reinforcement.