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Heterogeneity in Drosophila Signaling Systems

Abstract

Many biological systems are composed of heterogeneous elements. This work analyzes the heterogeneities found in signaling systems within the Drosophila nervous system, focusing on the neuromuscular junction and the antennal lobe. The variations found within each system are used to understand some aspect of its organization.

At the Drosophila larval neuromuscular junction (NMJ), a motor neuron releases glutamate from many boutons onto the muscle it innervates. A post-synaptically localizing calcium sensor was developed to visualize the distribution of synaptic strength across boutons. While the Ca2+ signals were uniform within a given connection (i.e., bouton and postsynapse pair), they differed considerably among connections of an NMJ. A gradient of transmission strength was observed along axonal branches, from weak proximal connections to strong distal ones. Presynaptic imaging revealed a matching axonal gradient, with higher Ca2+ influx and exocytosis at distal boutons. The results suggest that transmission strength is mainly determined presynaptically at the level of individual boutons, possibly by one or more factors existing in a gradient.

The antennal lobe (AL) is a structure that processes odors. It is partitioned into glomeruli, each of whose inputs detect unique chemical features. How specialized is the circuitry of each glomerulus to operate on its inputs? We utilize a methodology that allows a simultaneous, unbiased comparison of the functional organization of many glomeruli. We find that the glomerulus DA1, which is selectively activated by a single pheromone, is organized differently than glomeruli that are activated by many different odorants. In contrast to what is seen in other glomeruli, ipsilateral and contralateral stimuli elicit distinct spatial patterns of activity within DA1. DA1 experiences greater and more rapid inhibition than other glomeruli, allowing it to report slight inter-antennal delays in stimulus onset in a "winner-take-all" manner. We propose that DA1's specializations help the fly localize and orient with respect to pheromone sources. Our results show how homologous circuits reflect the unique contingencies of their inputs.

Together, these works show how the heterogeneity found within diverse systems can provide a basis for understanding their organization.

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