Maturing neurons and dual structural plasticity enable flexibility and stability of olfactory memory

The capacities to learn and to store memories are two of the most important functions of the brain, but these abilities are inherently at odds with each other. On one hand, a neuronal network must be flexible enough to quickly store new information, but on the other it must be stable enough to prevent old memories from being constantly overwritten. Metaplasticity in which the timescale of synaptic modifications made by an individual neuron changes could resolve this flexibility-stability tradeoff. We propose that this strategy may be implemented in the olfactory bulb (OB). A striking, characteristic feature of olfaction is that throughout adulthood new, initially highly plastic adult-born interneurons (abGCs) are added to the OB, while others are removed through well-controlled apoptosis. The computational benefit of this expensive form of plasticity is still poorly understood. Here, we use a biophysically inspired computational model of the rodent OB to show explicitly how neurogenesis, apoptosis, and established properties of abGCs, particularly their transiently enhanced excitability and structural plasticity, combine to enable the flexible formation of stable odor memories. The model demonstrates that all three components, neurogenesis, apoptosis and transient properties of abGCs, are necessary to achieve this goal. Moreover, in line with experiments, we show how memories are encoded by young abGCs, how these memories are briefly vulnerable to interference from a new stimulus, how re-learning a lost memory is faster than learning a new memory, and how the OB can learn several odors at the same time. The model predicts that odor exposure leads to the formation of birthdate-dependent, odor-specific subnetworks in the OB.