Abstract
BackgroundOdors are detected by sensory neurons that carry information to the olfactory lobe where they connect to projection neurons and local interneurons in glomeruli: anatomically well-characterized structures that collect, integrate and relay information to higher centers. Recent studies have revealed that the sensitivity of such networks can be modulated by wide-field feedback neurons. The connectivity and function of such feedback neurons are themselves subject to alteration by external cues, such as hormones, stress, or experience. Very little is known about how this class of central neurons changes its anatomical properties to perform functions in altered developmental contexts. A mechanistic understanding of how central neurons change their anatomy to meet new functional requirements will benefit greatly from the establishment of a model preparation where cellular and molecular changes can be examined in an identified central neuron.ResultsIn this study, we examine a wide-field serotonergic neuron in the Drosophila olfactory pathway and map the dramatic changes that it undergoes from larva to adult. We show that expression of a dominant-negative form of the ecdysterone receptor prevents remodeling. We further use different transgenic constructs to silence neuronal activity and report defects in the morphology of the adult-specific dendritic trees. The branching of the presynaptic axonal arbors is regulated by mechanisms that affect axon growth and retrograde transport. The neuron develops its normal morphology in the absence of sensory input to the antennal lobe, or of the mushroom bodies. However, ablation of its presumptive postsynaptic partners, the projection neurons and/or local interneurons, affects the growth and branching of terminal arbors.ConclusionOur studies establish a cellular system for studying remodeling of a central neuromodulatory feedback neuron and also identify key elements in this process. Understanding the morphogenesis of such neurons, which have been shown in other systems to modulate the sensitivity and directionality of response to odors, links anatomy to the development of olfactory behavior.
Highlights
Odors are detected by sensory neurons that carry information to the olfactory lobe where they connect to projection neurons and local interneurons in glomeruli: anatomically well-characterized structures that collect, integrate and relay information to higher centers
The contralaterally projecting serotonin-immunoreactive deutocerebral (CSD) interneuron is labeled by a flip-out technique We dissected brains of RN2-Flp, Tub-Flip Recombinase Target (FRT)-CD2-FRT-Gal4, UAS-mCD8GFP animals reared at 25°C and stained them with antibodies against green fluorescence protein (GFP; Figure 1a)
'Flippase' activity regulated by the RN2 promoter induces Flip Recombinase Target (FRT)-mediated recombination, leading to GFP expression in a small number of neurons in the adult central nervous system under Tub-Gal4 control (Additional file 1)
Summary
Odors are detected by sensory neurons that carry information to the olfactory lobe where they connect to projection neurons and local interneurons in glomeruli: anatomically well-characterized structures that collect, integrate and relay information to higher centers. Olfactory receptor neurons (ORNs) map, in a receptorspecific manner, from the antenna to glomeruli within the antennal lobes [2,3] They synapse onto projection interneurons (PNs) that, in turn, wire to dendritic fields of the mushroom bodies and the lateral horn of the protocerebrum [4]. Further evidence for the role of lateral excitation within the circuit was obtained by silencing all ORNs wiring to a single glomerulus and recording stimulus-evoked activity from the corresponding PNs [10] These systematic studies suggest the presence of crosstalk that couples most, if not all, glomeruli to each other. Further cellular computation could be achieved through the activity of wide-field feedback neurons that connect the higher centers with the antennal lobes [12,13]
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