The Morphological Identity of Insect Dendrites

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Abstract
Dendrite morphology, a neuron's anatomical fingerprint, is a neuroscientist's asset in unveiling organizational principles in the brain. However, the genetic program encoding the morphological identity of a single dendrite remains a mystery. In order to obtain a formal understanding of dendritic branching, we studied distributions of morphological parameters in a group of four individually identifiable neurons of the fly visual system. We found that parameters relating to the branching topology were similar throughout all cells. Only parameters relating to the area covered by the dendrite were cell type specific. With these areas, artificial dendrites were grown based on optimization principles minimizing the amount of wiring and maximizing synaptic democracy. Although the same branching rule was used for all cells, this yielded dendritic structures virtually indistinguishable from their real counterparts. From these principles we derived a fully-automated model-based neuron reconstruction procedure validating the artificial branching rule. In conclusion, we suggest that the genetic program implementing neuronal branching could be constant in all cells whereas the one responsible for the dendrite spanning field should be cell specific. Neural computation has been shown to be heavily dependent not only on the connectivity of single neurons but also on their specific dendritic shape—often used as a key feature for their classification. Still, very little is known about the constraints determining a neuron's morphological identity. In particular, one would like to understand what cells with the same or similar function share anatomically, what renders them different from others, and whether one can formalize this difference objectively. A large number of approaches have been proposed, trying to put dendritic morphology in a parametric frame. A central problem lies in the wide variety and variability of dendritic branching and function even within one narrow cell class. We addressed this problem by investigating functionally and anatomically highly conserved neurons in the fly brain, where each neuron can easily be individually identified in different animals. Our analysis shows that the pattern of dendritic branching is not unique in any particular cell, only the features of the area that the dendrites cover allow a clear classification. This leads to the conclusion that all fly dendrites share the same growth program but a neuron's dendritic field shape, its “anatomical receptive field”, is key to its specific identity.