Wiring Economy and Volume Exclusion Determine Neuronal Placement in the Drosophila Brain

Abstract

Wiring economy has successfully explained the individual placement of neurons in simple nervous systems like that of Caenorhabditis elegans [1-3] and the locations of coarser structures like cortical areas in complex vertebrate brains [4]. However, it remains unclear whether wiring economy can explain the placement of individual neurons in brains larger than that of C. elegans. Indeed, given the greater number of neuronal interconnections in larger brains, simply minimizing the length of connections results in unrealistic configurations, with multiple neurons occupying the same position in space. Avoiding such configurations, or volume exclusion, repels neurons from each other, thus counteracting wiring economy. Here we test whether wiring economy together with volume exclusion can explain the placement of neurons in a module of the Drosophila melanogaster brain known as lamina cartridge [5-13]. We used newly developed techniques for semiautomated reconstruction from serial electron microscopy (EM) [14] to obtain the shapes of neurons, the location of synapses, and the resultant synaptic connectivity. We show that wiring length minimization and volume exclusion together can explain the structure of the lamina microcircuit. Therefore, even in brains larger than that of C. elegans, at least for some circuits, optimization can play an important role in individual neuron placement.

Neuronal energy consumption: biophysics, efficiency and evolution

“…Consistent with this the placement of components within nervous systems is close to a configuration that minimizes the volume of wire at various scales from individual neurons [64][65][66] to brain regions [67,68]. Perhaps the clearest example of this wiring economy is in the layout of the C. elegans nervous system, where the positions of neurons show a striking match to the wire length minimized structure [6,64].…”

“…Perhaps the clearest example of this wiring economy is in the layout of the C. elegans nervous system, where the positions of neurons show a striking match to the wire length minimized structure [6,64]. More recent studies have shown that, the positions of neurons within more complex neural networks in insects adhere to a wire length minimized layout when the volume of the components is considered (volume exclusion) [65]. It has also been suggested that wiring economy can explain the difference in the position of the soma in invertebrate and vertebrate neurons [66].…”

“…This extends from the size and structure of single neurons [12,42,43,61] and neural tracts [62,63], to the placement of neurons within neural networks or regions within the cortex [e.g. [64][65][66][67][68]. Size is a key factor in determining neuronal energy consumption and the energy efficiency of information processing.…”

Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system

“…Studies using genetic methods for single-cell labeling have confirmed many of these cell types and newly identified others (8,9). For ∼60 cell types in two optic lobe subregions, the lamina and medulla, their synaptic connectivity has been revealed through serial-section electron microscopy (EM) (10)(11)(12)(13). Cell types that have arbors that span only one or a few medulla columns have been the easiest to characterize.…”

Micro-, Meso- and Macro-Connectomics of the Brain

“…Studies of microscale wiring patterns in Drosophila have demonstrated that the topology of specific subcircuits can be explained on the basis of wiring length minimization and volume exclusion, both mechanisms directed at the economical conservation of space (Rivera-Alba et al 2011). In a more recent electron microscopic study, Takemura et al (2013) reconstructed a microscale circuit comprising 379 neurons and 8637 synapses within the optic medulla, a structure involved in visual motion detection.…”