Abstract
Temporal experience of odor gradients is important in spatial orientation of animals. The fruit fly Drosophila melanogaster exhibits robust odor-guided behaviors in an odor gradient field. In order to investigate how early olfactory circuits process temporal variation of olfactory stimuli, we subjected flies to precisely defined odor concentration waveforms and examined spike patterns of olfactory sensory neurons (OSNs) and projection neurons (PNs). We found a significant temporal transformation between OSN and PN spike patterns, manifested by the PN output strongly signaling the OSN spike rate and its rate of change. A simple two-dimensional model admitting the OSN spike rate and its rate of change as inputs closely predicted the PN output. When cascaded with the rate-of-change encoding by OSNs, PNs primarily signal the acceleration and the rate of change of dynamic odor stimuli to higher brain centers, thereby enabling animals to reliably respond to the onsets of odor concentrations.
Highlights
Various odor concentration profiles were designed and tested (Figure 1—figure supplement 1), and the corresponding olfactory sensory neurons (OSNs) and projection neurons (PNs) responses were measured in two separate assays sharing the same odor delivery system (Figure 1A,B)
We tested a pair of directly connected OSNs and PNs innervating the DM4 glomerulus with five different acetone concentration waveforms
The dynamics of OSN and PN responses differed significantly from their respective feedforward inputs, and all responses initiated within a few tens of milliseconds of the odor onset (Figure 1C)
Summary
Odor distribution in nature is intermittent and dynamic (Murlis et al, 1992; Vickers et al, 2001), and animals have evolved the ability to detect and respond to temporal variation of odor stimuli (David et al, 1983; Thesen et al, 1993; Vickers et al, 2001; Porter et al, 2007; Semmelhack and Wang, 2009; Kato et al, 2014). Several recent studies have investigated how dynamic olfactory stimuli are processed in insect early olfactory systems (systems consisting principally of OSNs and projection neurons [PNs]) and observed significant temporal processing of odor signals (Bhandawat et al, 2007; Geffen et al, 2009; Kim et al, 2011; Nagel and Wilson, 2011; Martelli et al, 2013). Most of these studies employed a simple odor delivery system that generated step-pulse-like odor stimuli without directly monitoring the actual odor concentration levels. Natural odor plumes are encountered in various spatiotemporal patterns, and their dynamics and statistics can influence the neural encoding mechanism (Brenner et al, 2000; Vickers et al, 2001)
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