Analysis of structural plasticity in microglomerular synaptic circuits of the honeybee mushroom-bodies after sensory experience

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Division of labor among workers is a key feature of honeybee societies. Based on an age-related polyethism, young workers perform tasks inside the hive before starting to forage outside. This prominent behavioral transition exposes bees to new environments and places demands on bee cognition for spatial navigation, and identifying and memorizing profitable food sources in an ever-changing olfactory and visual environment. Neuronal substrates for accommodating changes in the sensory environment are the mushroom bodies (MBs), multimodal sensory integration centers important for learning and the formation of associative memories. They receive multimodal (olfactory and visual) input from cholinergic projection neurons (PNs) relayed to numerous MB intrinsic neurons (Kenyon cells, KCs) within morphologically elaborate (doubled and cup-shaped) MB calyces. PNs synapse on KCs forming large identifiable synaptic complexes called microglomeruli (MG). 3D quantitative imaging of PN boutons revealed a remarkable plasticity in PN bouton densities associated with variations in behavior as well as learning and memory processes on an individual level. Such changes are not only triggered by sensory stimuli but are also linked to age- and task-related behavioral maturation processes. This project aims to link changes in sensory experience with structural changes in neuronal circuit organization in the MB calyx. We focus in particular on the number of synapses and the types of their synaptic partners at the level of individual MG. How do the two different classes of MB KCs (spiny and clawed KCs) described for honeybees contribute to the circuitry of individual MG in the MB calyx? To study this question, we will conduct neurotracing in combination with 3D deep tissue imaging to label single or small subsets of KCs. We then aim to investigate how this connectivity is shaped by non-associative and associative sensory experience. How do sensory exposure and long-term memory (LTM) formation shape the connectivity between PN boutons and KC dendrites in the MB calyx? Do vesicle cargos and the number of active zones within PN boutons as well as numbers of postsynaptic profiles per active zone change after sensory exposure and LTM formation? To address this issue, we will apply advanced EM techniques (serial block face scanning microscopy and electron microscopy) to analyze structural plasticity of the pre- and postsynaptic organization of individual MG at high resolution. We hypothesize that a reorganization of synaptic MG at the MB input adjusts divergence ratios between PNs and KCs. We expect that our findings reveal important insights into the structural plasticity of neuronal circuits that accompany sensory experience-related changes in olfactory and visual processing in the honeybee.