Distinct forms of structural plasticity of adult-born interneuron spines induced by different odor learning paradigms

During development and in adulthood the morpho-functional properties of neural networks constantly adapt in response to environmental stimuli and learned experiences. One of the processes that allows neuronal networks to be constantly reshaped is synaptic plasticity, which is induced in response to sensory experience and learning. Synaptic plasticity allows for the formation/elimination of synaptic connections as well as the strengthening of pre-existing ones. The olfactory system is particularly prone to constant morpho-functional reshaping of neural networks and synaptic rewiring throughout the lifespan of an animal, mainly because of the presence of continuous neurogenesis in the olfactory bulb (OB). This constant synaptic rewiring brought by adult-born neurons is modulated by the level of odor-induced activity and olfactory learning. It remains, however, unclear whether the complexity of distinct odor-induced learning paradigms and sensory stimulation induces different forms of structural plasticity. In the present study, we developed an analytical pipeline to perform 3D reconstructions of spines from confocal images followed by clustering of reconstructed spines based on different morphometric features and in relationship with different sensory stimuli and learning paradigms. We show that while sensory deprivation decreased the overall density of adult-born neurons in the OB without any noticeable changes in the morphometric properties of these spines, simple and complex odor learning paradigms triggered distinct forms of structural plasticity. A simple odor learning task affected the morphometric properties of the spines without any changes in spine density, whereas a complex odor learning task induced changes in spine density, without substantial changes in the morphology of the spines. Our work reveals the vast panoply of distinct forms of synaptic plasticity of adult-born neurons in the OB tailored to the complexity of odor-learning paradigms and sensory inputs.