Abstract
Drosophila olfactory local interneurons (LNs) in the antennal lobe are highly diverse and variable. How and when distinct types of LNs emerge, differentiate, and integrate into the olfactory circuit is unknown. Through systematic developmental analyses, we found that LNs are recruited to the adult olfactory circuit in three groups. Group 1 LNs are residual larval LNs. Group 2 are adult-specific LNs that emerge before cognate sensory and projection neurons establish synaptic specificity, and Group 3 LNs emerge after synaptic specificity is established. Group 1 larval LNs are selectively reintegrated into the adult circuit through pruning and re-extension of processes to distinct regions of the antennal lobe, while others die during metamorphosis. Precise temporal control of this pruning and cell death shapes the global organization of the adult antennal lobe. Our findings provide a road map to understand how LNs develop and contribute to constructing the olfactory circuit.
Highlights
Developmental or postnatal defects in interneurons have long been associated with neurological disorders[1,2], yet the diversity of these cells makes studying their development and functions in normal and pathological conditions extremely challenging[3,4,5,6,7]
The initial screen identified 109 candidate local interneurons (LNs) GAL4 lines, which were subjected to a second round of screening, wherein brains were costained for nuclear lacZ or γ-aminobutyric acid[31] to characterize the number of labeled LNs, their morphologies, and their identities as GABAergic or non-GABAergic neurons
Focusing on 15 LN GAL4 lines from the screen and 4 known LN GAL4 lines (189Y, NP3056, LCCH3-GAL44, and krasavietz4,16), we systematically examined the development of distinct subsets of LNs by analyzing their innervation patterns at 9–12 developmental time points (Fig. 2 and Supplementary Fig. 1)
Summary
Developmental or postnatal defects in interneurons have long been associated with neurological disorders[1,2], yet the diversity of these cells makes studying their development and functions in normal and pathological conditions extremely challenging[3,4,5,6,7]. Interneurons are continuously generated from the postnatal stage to adulthood and sequentially integrate into existing mature circuits[9,10] All of these features add complexity to wiring principles of interneurons. In addition to the differences between cells, the molecular properties and morphologies of individual LNs may change in response to alterations in environmental stimuli, such as different food sources or CO2-containing stress odor[24,25,26]. Because these characteristics of interneurons are similar among many species, Drosophila olfactory LNs may serve as a model to reveal common mechanisms of interneuron development and wiring principles. Controlled pruning and degeneration of LN processes contributes to shaping the global organization and characteristic positions of glomeruli a b
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