Olfactory Object Recognition Based on Fine-Scale Stimulus Timing in Drosophila

Abstract

Summary Odorants of behaviorally relevant objects (e.g., food sources) intermingle with those from other sources. Therefore to determine whether an odor source is good or bad—without actually visiting it—animals first need to segregate the odorants from different sources. To do so, animals could use temporal stimulus cues, because odorants from one source exhibit correlated fluctuations, whereas odorants from different sources are less correlated. However, the behaviorally relevant timescales of temporal stimulus cues for odor source segregation remain unclear. Using behavioral experiments with free-flying flies, we show that (1) odorant onset asynchrony increases flies' attraction to a mixture of two odorants with opposing innate or learned valence and (2) attraction does not increase when the attractive odorant arrives first. These data suggest that flies can use stimulus onset asynchrony for odor source segregation and imply temporally precise neural mechanisms for encoding odors and for segregating them into distinct objects.

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

“…We found that stimulus onset asynchronies of 5 seconds or more improved odor-background segregation, while stimulus onset asynchronies of 1 seconds or less did not. This timescale for segregating unknown odorants based on stimulus onset asynchrony is at least two orders of magnitude slower than for segregating known odorants (Baker et al, 1998;Sehdev et al, 2019;Szyszka et al, 2012). These results suggest that the neural mechanisms for odor-background segregation based on stimulus onset asynchrony differ for known and unknown odorants.…”

“…Because stimulus onset asynchrony can improve odor-background segregation for known target odorants (Andersson et al, 2011;Baker et al, 1998;Hopfield and Gelperin, 1989;Sehdev et al, 2019;Szyszka et al, 2012), we asked whether mixing A with an asynchronous background would still impair the recognition of A in a mixture with B. We presented B for 30 s and added a 7 s long target odorant A after 20 s (B20A; Fig.…”

“…Besides this trial-to-trial variability of odorant concentration or composition, animals can also use stimulus onset asynchrony between mixed odorants for segregating odorants from mixtures (Andersson et al, 2011;Baker et al, 1998;Hopfield and Gelperin, 1989;Saha et al, 2013;Sehdev et al, 2019;Szyszka et al, 2012;Weissburg et al, 2012). However, so far, this capability has only been demonstrated for known odorants that had either an innate or learned valence.…”

“…In particular, odorants that arise from a single source would arrive at the olfactory organ synchronously, whereas odorants that arise from multiple sources would differ in their arrival times (Erskine et al, 2019;Hopfield, 1991). Accordingly, invertebrates can use both spatial and temporal information from odor plumes for odor-background segregation (spatial: (Andersson et al, 2011;Baker et al, 1998;Hopfield and Gelperin, 1989;Weissburg et al, 2012); temporal: (Saha et al, 2013;Sehdev et al, 2019;Szyszka et al, 2012). Remarkably, tobacco hawk moths can segregate odorant sources separated by only 1 millimeter (Baker et al, 1998), and honey bees can use odorant onset asynchronies as short as 6 milliseconds to segregate a known target odorant (odorant with innate or learned valence) from a background odorant (Szyszka et al, 2012).…”

“…All previous studies that have investigated odor segregation based on temporal stimulus cues have in common that the target odorant was known to the animal, either through having an innate valence (Andersson et al, 2011;Baker et al, 1998;Nikonov and Leal, 2002;Weissburg et al, 2012) or via appetitive conditioning (Hopfield and Gelperin, 1989;Saha et al, 2013;Sehdev et al, 2019;Szyszka et al, 2012). It is currently unknown whether animals can use temporal stimulus cues to segregate an unknown odorant (odorant without innate or learned valence) from a background without ever encountering the target odorant alone.…”