Comparative Connectomics Highlights Conserved Architectural Synaptic Motifs in the Drosophila Mushroom Body

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ABSTRACT While the influence of synaptic plasticity on learning and memory has been extensively studied, the detailed patterns of synaptic connectivity remain incompletely mapped. Convergent synaptic motifs — a tight grouping of at least two axons whose active zones are within 300nm and which are presynaptic to the same target — are a common feature of neural circuits in the insect brain and are believed to serve as an important computational primitive in many brain areas. The Mushroom Body (MB) of Drosophila , for instance, is the center of associative learning and memory, where sensory information is conducted by Kenyon cells (KCs), the intrinsic neurons of the MB, and integrated by MB output neurons (MBONs). Indeed, the majority of KC-to-MBON synapses occur in a convergent motif. Nonetheless, the functional role of this convergent motif is not well studied. To gain insight into their potential role in the MB, we combine big-data network neuroscience tools with existing electron microscopy connectome datasets to detect and map the distribution of convergent synaptic motifs. We find that convergent motifs consistently occur across the MB in different individuals, including the α -lobe where they were first quantified, and we report on both the variance and consistency in the formation of these motifs across different MB regions and individuals. Our discovery of multiply-convergent motifs — where two KCs target multiple postsynaptic targets simultaneously — reveals a previously unrecognized synaptic economy that may optimize information transfer while conserving neural resources. These stereotyped arrangements likely represent fundamental organizational principles underlying associative learning across species. Lastly, to our knowledge, this study offers the first and most extensive comparative analysis of synaptic motifs across Drosophila connectomes, establishing a framework for enabling systematic motif analysis of synapses across species.

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