Distinct ultrastructural properties and plasticity of synapses formed by adult-born and early-born interneurons in the mouse olfactory bulb

The olfactory bulb (OB) is one of the few regions in the adult brain that receives newly generated neuronal precursors throughout the lifespan of animals. These neuronal precursors differentiate into OB interneurons, mostly granule cells (GCs), and integrate into the bulbar network by forming dendro-dendritic reciprocal synapses with OB principal neurons. The ultrastructural properties and plasticity of these synapses and whether they are distinct from those formed by early-born, resident GCs remain unknown. In the present study, we assessed the ultrastructural properties of dendro-dendritic reciprocal synapses formed by either adult-born or resident, early-born GCs with principal neurons in mice of both sexes and studied their plasticity following sensory deprivation and odor learning. The synapses formed by either adult-born or resident, early-born GCs with principal bulbar neurons were undistinguishable in terms of area, diameter, and aspect ratio. In contrast, the synapses formed by adult-born GCs were characterized by a smaller synaptic cleft and a larger density of total and docked synaptic vesicles than synapses formed by resident GCs. Sensory deprivation and odor learning decreased and increased, respectively, the overall density and the number of docked synaptic vesicles in adult-born and resident GCs forming synapses with principal neurons. Our results revealed important differences in the ultrastructural properties of synapses formed by interneurons born at distinct developmental stages and revealed their plasticity in response to sensory deprivation and odor learning. Significance Statement The adult-born neurons in the olfactory bulb play an important role in the bulbar network functioning and odor behavior. In this work, we characterized the ultrastructural properties of synapses formed by adult-born and resident or early-born interneurons with bulbar principal cells and assessed their plasticity following sensory deprivation and odor learning. We revealed marked differences in synapses formed by adult-born interneurons that are characterized by increased density of synaptic vesicles and higher number of docked vesicles as compared to synapses formed by resident, early-born interneurons. We also showed their plasticity following sensory deprivation and odor learning. Our data provide insights for exquisite implication of adult-born interneurons in the odor information processing and odor behavior.