Abstract
Innate attraction and aversion to odorants are observed throughout the animal kingdom, but how olfactory circuits encode such valences is not well understood, despite extensive anatomical and functional knowledge. In Drosophila melanogaster, ~50 types of olfactory receptor neurons (ORNs) each express a unique receptor gene, and relay information to a cognate type of projection neurons (PNs). To examine the extent to which the population activity of ORNs is required for olfactory behavior, we developed a genetic strategy to block all ORN outputs, and then to restore output in specific types. Unlike attraction, aversion was unaffected by simultaneous silencing of many ORNs, and even single ORN types previously shown to convey neutral valence sufficed to mediate aversion. Thus, aversion may rely on specific activity patterns in individual ORNs rather than the number or identity of activated ORNs. ORN activity is relayed into the brain by downstream circuits, with excitatory PNs (ePN) representing a major output. We found that silencing the majority of ePNs did not affect aversion, even when ePNs directly downstream of single restored ORN types were silenced. Our data demonstrate the robustness of olfactory aversion, and suggest that its circuit mechanism is qualitatively different from attraction.
Highlights
Olfactory circuits in insects and mammals exhibit striking functional and anatomical similarities [1]
olfactory receptor neurons (ORNs) can be divided into two classes expressing either an odorant receptor (OR) or an ionotropic receptor (IR)
The major component of vinegar, preferentially activates the Ir8a-expressing subset of IR + ORNs [8], we examined Ir8a > shits1 flies [28], and found that they were less attracted to vinegar (Fig 1B)
Summary
Olfactory circuits in insects and mammals exhibit striking functional and anatomical similarities [1]. Olfactory inputs are high dimensional, corresponding to the activation patterns of ~50 types of olfactory receptor neurons (ORNs) in flies and ~1000 ORN types in mice. Among these input channels, a minority are “specialists”, responding to one odorant or one category of odorants [2,3,4]. ORNs of the same type express the same receptor, and project to the same glomerulus in the antennal lobes in flies [6,7,8] or olfactory bulbs in mice [9, 10]; each projection neuron (PN) in flies or mitral/tufted cell in mice relays information from a PLOS ONE | DOI:10.1371/journal.pone.0125986. ORNs of the same type express the same receptor, and project to the same glomerulus in the antennal lobes in flies [6,7,8] or olfactory bulbs in mice [9, 10]; each projection neuron (PN) in flies or mitral/tufted cell in mice relays information from a PLOS ONE | DOI:10.1371/journal.pone.0125986 April 30, 2015
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