Complementary Function and Integrated Wiring of the Evolutionarily Distinct Drosophila Olfactory Subsystems

By Ana F. Silbering, R. Rytz, Y. Grosjean, L. Abuin, Pavan Ramdya, Gregory S. X. E. Jefferis, Richard Benton. 2011

472 citations recorded by the source corpus.

To sense myriad environmental odors, animals have evolved multiple, large families of divergent olfactory receptors. How and why distinct receptor repertoires and their associated circuits are functionally and anatomically integrated is essentially unknown. We have addressed these questions through comprehensive comparative analysis of the Drosophila olfactory subsystems that express the ionotropic receptors (IRs) and odorant receptors (ORs). We identify ligands for most IR neuron classes, revealing their specificity for select amines and acids, which complements the broader tuning of ORs for esters and alcohols. IR and OR sensory neurons exhibit glomerular convergence in segregated, although interconnected, zones of the primary olfactory center, but these circuits are extensively interdigitated in higher brain regions. Consistently, behavioral responses to odors arise from an interplay between IR- and OR-dependent pathways. We integrate knowledge on the different phylogenetic and developmental properties of these receptors and circuits to propose models for the functional contributions and evolution of these distinct olfactory subsystems.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Sensory Systems

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Citations in the corpus

Organization of antennal lobe‐associated neurons in adult Drosophila melanogaster brain (2012, background): “…and send projections to one of about 50 glomeruli in the AL (Stocker, 1994; Laissue et al., 1999; Clyne et al., 1999; Gao and Chess, 1999; Vosshall et al., 2000; Scott et al., 2001; Stortkuhl and Kettler, 2001; Wetzel et al., 2001; Larsson et al., 2004; Benton et al., 2009; Silbering et al., 2011).”
A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster (2017, background): “, 2015); our reconstructions indicated clear independent domains for VC3l and VC3m glomeruli (consistent with Chou et al., 2010; Silbering et al., 2011); and VC3l and VC5 could not be disambiguated.”
Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system (2013, background): “Some of the ORNs innervating this region are narrowly tuned to organic acids (17).”
Non-Canonical Odor Coding in the Mosquito (2020, background): “The Drosophila melanogaster orthologues, Ir41a, Ir76a, and Ir92a, have all been shown to compose channels that respond to amines (Hussain et al., 2016; Min et al., 2013; Silbering et al., 2011).”
Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing (2015, background): “Ors, which respond broadly to alcohols, ketones, and esters, Irs primarily respond to acids, amines, and carbon dioxide, which can be physiologically important in many insect species [77,86-88].”
Insect olfaction and the evolution of receptor tuning (2015, unknown): “…the periphery, alterations in regulatory genes controlling receptor gene expression (Ray et al., 2008), as well as potential modulation of neuronal circuits, structures, and processing mechanisms in the brain (Couto et al., 2005; Ramdya and Benton, 2010; Silbering et al., 2011; Cande et al., 2013).”