Short-term availability of adult-born neurons for memory encoding

Jérémy Forest,Anne Didier,Matthias Cavelius,Mélissa Moreno,Laura Chalençon,Joëlle Sacquet,Marion Richard,Nathalie Mandairon,Anne Ziessel

doi:10.1038/s41467-019-13521-7

Jérémy Forest, Anne Didier + Show 7 more

Open Access

https://doi.org/10.1038/s41467-019-13521-7

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Abstract

Adult olfactory neurogenesis provides waves of new neurons involved in memory encoding. However, how the olfactory bulb deals with neuronal renewal to ensure the persistence of pertinent memories and the flexibility to integrate new events remains unanswered. To address this issue, mice performed two successive olfactory discrimination learning tasks with varying times between tasks. We show that with a short time between tasks, adult-born neurons supporting the first learning task appear to be highly sensitive to interference. Furthermore, targeting these neurons using selective light-induced inhibition altered memory of this first task without affecting that of the second, suggesting that neurons in their critical period of integration may only support one memory trace. A longer period between the two tasks allowed for an increased resilience to interference. Hence, newly formed adult-born neurons regulate the transience or persistence of a memory as a function of information relevance and retrograde interference.

Highlights

Adult olfactory neurogenesis provides waves of new neurons involved in memory encoding
Using the olfactory system in mice, we tackle the issue of how the acquisition of new memories influences the information already stored in the network and we identify the role of adultborn neurons in these processes
We used perceptual olfactory discrimination learning, which depends on newly formed neurons in the OB8 to show that (1) adult-born neurons saved by learning are present in the olfactory bulb (OB) as long as the task is remembered; (2) with a second learning task occurring soon after the first, introducing retrograde interference, the new memory overwrites the older one and alters survival of previously recruited adultborn neurons unless (3) the first learned odorants are maintained in the environment

Summary

Introduction

Adult olfactory neurogenesis provides waves of new neurons involved in memory encoding. How the olfactory bulb deals with neuronal renewal to ensure the persistence of pertinent memories and the flexibility to integrate new events remains unanswered To address this issue, mice performed two successive olfactory discrimination learning tasks with varying times between tasks. The neuronal turnover provided by adult neurogenesis could sub-serve memory formation and regulate the transience of the memory trace This raises the issue of how this ‘remembering/ forgetting’ balance is regulated as a function of environmental demand, allowing the animal to keep relevant information in memory for optimal behavioral adaptation. We used perceptual olfactory discrimination learning, which depends on newly formed neurons in the OB8 to show that (1) adult-born neurons saved by learning are present in the OB as long as the task is remembered; (2) with a second learning task occurring soon after the first, introducing retrograde interference, the new memory overwrites the older one and alters survival of previously recruited adultborn neurons unless (3) the first learned odorants are maintained in the environment. Using sequential labeling of adultborn neurons and selective optogenetic inactivation, we showed (4) that each successive learning is supported by a specific population of adult-born neurons

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