Dissecting the neuronal mechanisms of memory consolidation during sleep

Dissecting the neuronal mechanisms of memory consolidation during sleep


By Vincenzo Mastrolia, King's College London

Dr Gabrielle Girardeau, of the INSERM Institut du Fer à Moulin (IFM) in Paris, gave a seminar as part of the 2020/21 “NEUReka!” seminar series. Dr Girardeau’s research focuses on the processing of memory during sleep and their link with emotions and anxiety.

During her seminar, Dr Girardeau presented the fantastic work she has completed during her career, starting from her PhD/Postdoc period at the Zugaro lab in the Collège de France (Paris), moving on to her postdoc in the Buzsaki lab at the NYU Neuroscience Institute/Langone Medical Center (New York), and finally opening up her own lab at the IFM (Paris).

NEUReka! Seminar Series
NEUReka! Seminar Series

The processing of spatial and episodic memories relies on an intricate neuronal network with the hippocampus at its centre. This brain region presents an extensive processing of inputs originating from a multitude of brain areas, both cortical and subcortical. It is therefore essential for the hippocampus to integrate and consolidate the load of information it receives.

Dr Gabrielle Girardeau (Principal Investigator)
Dr Gabrielle Girardeau (Principal Investigator)

Memory consolidation allows the information stored in the hippocampus to be transferred into more long‐lasting cortical areas.

During her years in the Zugaro lab, Dr Girardeau produced striking findings on the importance of sleep and Sharp‐Wave Ripples (SPW‐R) during memory consolidation. SPW‐R are short bursts of neuronal activity that can be distinguished in electrophysiological recordings during resting or sleeping epochs.

By using in vivo electrophysiological recordings combined with behavioural tasks, Dr Girardeau and Zugaro lab elegantly showed a causative role of SPW‐R in memory consolidation (Girardeau et al., 2009; Maingret et al., 2016). In order to do so, rats that performed a spatial memory behavioural task were let to sleep, while the activity of dorsal hippocampus was monitored using in vivo electrophysiology. The patterns of activity were analysed in real‐time, allowing the prompt detection of SPW‐R events. At the occurrence of each SWP‐R in the hippocampus, an electrical stimulus was delivered in the ventral hippocampal commissure, interrupting the complete development of the SPW‐R event. When repeating the same spatial memory task in the following days, the rats whose hippocampal SPW‐R events were suppressed during sleep needed extra days to succeed the spatial memory task, when compared to control rats with intact SPW‐R events.

The amygdala's pivotal importance in determining the intensity of emotions and their association with memories

During her postdoctoral experience in Buzsaki lab, Dr Girardeau produced fantastic results proving the importance of the interaction between the hippocampus and the amygdala during consolidation of emotional memories (Girardeau et al., 2017). In order to evaluate the connection between these two areas, rats were set to perform an aversive spatial memory task, where these animals had to pass through an air puff checkpoint (the aversive stimulus) in order to reach water. The position of the aversive stimulus was changed each day, and the capacity of the rats to remember their position from the previous day and to memorize the new position on the current day was measured as change in the animal’s moving speed before and after the location of the air puff.

Dr Girardeau and Buzsaki lab set the goal to measure the connection between the amygdala and the hippocampus, and their participation in the consolidation of aversive memory. In order to do so, they performed in vivo electrophysiological recordings of both the dorsal hippocampus and the amygdala, with particular attention in mapping the majority of neurons activating in the amygdala during the aversive memory task mentioned above. By looking at the variance of pairwise correlations between hippocampal and basolateral amygdala (BLA) neurons activating during sleep after the aversive memory task, Dr Girardeau showed reactivation of the same correlated group of neurons during the task. Moreover, a subset of BLA neurons showed a higher reactivation during the task. Dr Girardeau and Buzsaki lab showed that these neurons were positively modulated by hippocampal SPW‐R, confirming the connection between these two areas and the role for SPW‐R in consolidating aversive memories.

Conclusion

Now at the Institut du Fer à Moulin with her own lab, Dr Girardeau continues to work on the interaction between hippocampus and amygdala, and its impact on the processing of emotional memories and anxiety, using in vivo electrophysiological and optogenetic approaches. Her work will have an impactful effect on our understanding of memory formation.

References

Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009). Selective suppression of hippocampal ripples impairs spatial memory. Nature Neuroscience, 12(10), 1222–1223. https://doi.org/10.1038/nn.2384

Girardeau, G., Inema, I., & Buzsáki, G. (2017). Reactivations of emotional memory in the hippocampus‐amygdala system during sleep. Nature Neuroscience, 20(11), 1634–1642. https://doi.org/10.1038/nn.4637

Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016). Hippocampo‐cortical coupling mediates memory consolidation during sleep. Nature Neuroscience, 19(7), 959–964. https://doi.org/10.1038/nn.4304

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