Abstract
SummaryTaking advantage of the well-characterized olfactory system of Drosophila, we derive a simple quantitative relationship between patterns of odorant receptor activation, the resulting internal representations of odors, and odor discrimination. Second-order excitatory and inhibitory projection neurons (ePNs and iPNs) convey olfactory information to the lateral horn, a brain region implicated in innate odor-driven behaviors. We show that the distance between ePN activity patterns is the main determinant of a fly’s spontaneous discrimination behavior. Manipulations that silence subsets of ePNs have graded behavioral consequences, and effect sizes are predicted by changes in ePN distances. ePN distances predict only innate, not learned, behavior because the latter engages the mushroom body, which enables differentiated responses to even very similar odors. Inhibition from iPNs, which scales with olfactory stimulus strength, enhances innate discrimination of closely related odors, by imposing a high-pass filter on transmitter release from ePN terminals that increases the distance between odor representations.
Highlights
Most neurons involved in perceptual judgments are at least two synapses removed from sensory receptors
Second-order excitatory and inhibitory projection neurons convey olfactory information to the lateral horn, a brain region implicated in innate odor-driven behaviors
We show that the distance between excitatory projection neurons (ePNs) activity patterns is the main determinant of a fly’s spontaneous discrimination behavior
Summary
Most neurons involved in perceptual judgments are at least two synapses removed from sensory receptors. Psychophysical models that link perception to the physical qualities of external stimuli are black boxes: they do not account for how sensory information is encoded and how the resulting internal representations support the detection and discrimination of stimuli. Opening these black boxes has been difficult. The mean spike rates evoked by 110 odorants in 24 of the $50 ORN types of adult flies have been measured (Hallem and Carlson, 2006; Hallem et al, 2004), providing a quantitative description of activity in approximately half of the neuronal population at the input stage of the olfactory system
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