Multiple sites of adaptation lead to contrast encoding in theDrosophilaolfactory system

Abstract

Animals often encounter large increases in odor intensity that can persist for many seconds. These increases in the background odor are often accompanied by increases in the variance of the odor stimulus. Previous studies have shown that a persistent odor stimulus (odor background) results in a decrease in the response to brief odor pulses in the olfactory receptor neurons (ORNs). However, the contribution of adapting mechanisms beyond the ORNs is not clear. Thus, it is unclear how adaptive mechanisms are distributed within the olfactory circuit and what impact downstream adaptation may have on the encoding of odor stimuli. In this study, adaptation to the same odor stimulus is examined at multiple levels in the well studied and accessible Drosophila olfactory system. The responses of the ORNs are compared to the responses of the second order, projection neurons (PNs), directly connected to them. Adaptation in PN spike rate was found to be much greater than adaptation in the ORN spike rate. This greater adaptation allows PNs to encode odor contrast (ratio of pulse intensity to background intensity) with little ambiguity. Moreover, distinct neural mechanisms contribute to different aspects of adaptation; adaptation to the background odor is dominated by adaptation in spike generation in both ORNs and PNs, while adaptation to the odor pulse is dominated by changes within olfactory transduction and the glomerulus. These observations suggest that the olfactory system adapts at multiple sites to better match its response gain to stimulus statistics.

Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli

“…In olfaction, the Weber-Fechner Law was demonstrated at the LFP level (Cafaro, 2016; Cao et al, 2016). Here we directly measured ORN firing rate and stimulus intensity and found that the ORN firing rate exhibited Weber-Fechner gain scaling relative to the mean stimulus intensity for five different odor-receptor combinations (Figure 3, Figure 3—figure supplement 1).…”

Controlling and measuring dynamic odorant stimuli in the laboratory

“…Short pulses of odorants are usually used to estimate the dose-response curve of single neurons 6,24,26 . A simple way to generate odorant pulses of varying concentrations is to force air through cartridges containing odorants diluted to varying degrees in a solvent, like paraffin oil.…”

“…We aim to provide some intuition about why the output of the delivery system may not match expectations. Previous works have used either simple odor delivery systems that can generate simple stimuli, or custom-designed instruments capable of complex stimuli but that are challenging to engineer 6,[21][22][23][24] . Here, we describe methods to deliver complex and intermittent odorant stimuli using off-the-shelf components.…”

Odor-background segregation of unknown odorants based on stimulus onset asynchrony in honey bees

“…Similarly, insect olfactory receptor neurons and projection neurons (in Drosophila) adapt to a constant odorant stimulus (Bhandawat et al, 2007;Cafaro, 2016;de Bruyne et al, 2001;Martelli et al, 2013;Nagel and Wilson, 2011) but they remain responsive to a novel odorant pulse that arrives a few seconds after the onset of the background odorant (Cafaro, 2016). In honey bees, neural responses start adapting within a few hundreds of milliseconds (projection neurons: (Krofczik et al, 2009;Sachse and Galizia, 2002); Kenyon cells: (Farkhooi et al, 2013;Froese et al, 2014;Szyszka et al, 2005)).…”