Abstract

A comparison between the axon terminals of octopaminergic efferent dorsal or ventral unpaired median neurons in either desert locusts (Schistocerca gregaria) or fruit flies (Drosophila melanogaster) across skeletal muscles reveals many similarities. In both species the octopaminergic axon forms beaded fibers where the boutons or varicosities form type II terminals in contrast to the neuromuscular junction (NMJ) or type I terminals. These type II terminals are immunopositive for both tyramine and octopamine and, in contrast to the type I terminals, which possess clear synaptic vesicles, only contain dense core vesicles. These dense core vesicles contain octopamine as shown by immunogold methods. With respect to the cytomatrix and active zone peptides the type II terminals exhibit active zone-like accumulations of the scaffold protein Bruchpilot (BRP) only sparsely in contrast to the many accumulations of BRP identifying active zones of NMJ type I terminals. In the fruit fly larva marked dynamic changes of octopaminergic fibers have been reported after short starvation which not only affects the formation of new branches (“synaptopods”) but also affects the type I terminals or NMJs via octopamine-signaling (Koon et al., 2011). Our starvation experiments of Drosophila-larvae revealed a time-dependency of the formation of additional branches. Whereas after 2 h of starvation we find a decrease in “synaptopods”, the increase is significant after 6 h of starvation. In addition, we provide evidence that the release of octopamine from dendritic and/or axonal type II terminals uses a similar synaptic machinery to glutamate release from type I terminals of excitatory motor neurons. Indeed, blocking this canonical synaptic release machinery via RNAi induced downregulation of BRP in neurons with type II terminals leads to flight performance deficits similar to those observed for octopamine mutants or flies lacking this class of neurons (Brembs et al., 2007).

Highlights

  • Vertebrate skeletal muscle is innervated by excitatory cholinergic motor neurons

  • Muscle M85 consists of two parts and is innervated by two glutamatergic excitatory motor neurons (Pflüger et al, 1986), one GABAergic common inhibitor neuron (Wolf and Lang, 1994), and by an octopaminergic DUM3,4,5-neuron

  • The axonal terminals of the octopaminergic DUM3,4,5-neuron are labeled with an α-octopamine AB and appear very similar to the type II terminals of octopaminergic ventral unpaired median (VUM-)neurons of Drosophila larvae

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Summary

Introduction

Vertebrate skeletal muscle is innervated by excitatory cholinergic motor neurons. By contrast, insect skeletal muscle is innervated by glutamatergic excitatory motor neurons, and may receive additional innervation by inhibitory neurons and neuromodulatory neurons (Usherwood, 1975; Wolf and Lang, 1994; Pflüger and Duch, 2011). Some special peptidergic type III terminals were described (Anderson et al, 1988; Cantera and Nässel, 1992; Gorczyca et al, 1993; Zhong and Peña, 1995; Budnik, 1996), but the majority of axonal terminals of neuromodulatory neurons including octopaminergic neurons (Atwood et al, 1993; Monastirioti et al, 1995) consists of type II terminals In other insects these aminergic axons were described as ‘‘beaded fibers’’ because of the regular occurrence of varicosities or boutons along their length.

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