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Authors & Affiliations
Yewushuang Chen, Guangwei Si
Abstract
We hypothesize that the principle of wiring economy provides a compelling constraint for the spatial arrangement of Drosophila olfactory glomeruli. By comparing the wiring cost of actual glomerular organization with random configurations, we validated the role of wiring economy in shaping the spatial distribution of glomeruli. Building on this, we modeled three potential spatial organization strategies---the ‘onion’ model, the ‘orange’ model, and the ‘floor’ model---to compare the assembly strategy under the lens of wiring economy. Our calculations revealed that both the ‘floor’ and ‘orange’ models identified the same optimal gradient direction for assembly cue. Along this direction, the neural wiring cost was significantly lower than all other orientations, with the wiring cost increasing as the deviation from the optimal direction grew. The worst-case scenario resembled a near-random arrangement. To experimentally validate this theoretical calculation, we analyzed the three-dimensional concentration gradient of the axon guidance cue, semaphorin-1a (sema-1a), in the olfactory circuit using immunohistochemistry. Our measured 3D sema-1a gradient direction, agrees with the previously published 2D gradient direction, and showed a strong correlation of 0.69 with the predicted gradient direction. Our study not only confirms that wiring economy constrains the spatial arrangement of olfactory glomeruli, but also investigates the feasibility of applying this principle to predict the assembly processes of the neural circuits. As more connectome data are available, our approach extends the use of connectome datasets by combining them with first principles to elucidate neural circuit assembly strategies. This approach has broader implications, potentially guiding studies on the development of other brain regions in Drosophila and even across species.