Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation

Insects have a remarkable ability to identify and track odour sources in multi-odour backgrounds. Recent behavioural experiments show that this ability relies on detecting millisecond stimulus asynchronies between odourants that originate from different sources. Honeybees, Apis mellifera , are able to distinguish mixtures where both odourants arrive at the same time (synchronous mixtures) from those where odourant onsets are staggered (asynchronous mixtures) down to an onset delay of only 6 ms. In this paper we explore this surprising ability in a model of the insects' primary olfactory brain area, the antennal lobe. We hypothesize that a winner-take-all inhibitory network of local neurons in the antennal lobe has a symmetry-breaking effect, such that the response pattern in projection neurons to an asynchronous mixture is different from the response pattern to the corresponding synchronous mixture for an extended period of time beyond the initial odourant onset where the two mixture conditions actually differ. The prolonged difference between response patterns to synchronous and asynchronous mixtures could facilitate odour segregation in downstream circuits of the olfactory pathway. We present a detailed data-driven model of the bee antennal lobe that reproduces a large data set of experimentally observed physiological odour responses, successfully implements the hypothesised symmetry-breaking mechanism and so demonstrates that this mechanism is consistent with our current knowledge of the olfactory circuits in the bee brain

The Speed of Smell: Odor-Object Segregation within Milliseconds

Segregating objects from background, and determining which of many concurrent stimuli belong to the same object, remains one of the most challenging unsolved problems both in neuroscience and in technical applications. While this phenomenon has been investigated in depth in vision and audition it has hardly been investigated in olfaction. We found that for honeybees a 6-ms temporal difference in stimulus coherence is sufficient for odor-object segregation, showing that the temporal resolution of the olfactory system is much faster than previously thought

A 6-ms temporal difference in stimulus coherence is sufficient for odor-object segregation.

<p>(<b>a</b>) Each bee received 3 rewarded training trials with <i>A</i>, and the percentage of bees showing odor-evoked proboscis extension is shown. Odorant stimulus duration was 800 ms. During the memory test, odorants <i>A</i> and <i>B</i> were presented simultaneously (coherent mixture, <i>AB</i>) or with a 6-ms interval between their onsets (incoherent mixture). One incoherent mixture started with <i>A</i> (<i>A.B</i>), the other with <i>B</i> (<i>B.A</i>). Test stimulus sequence was randomized. The proboscis extension rate for the incoherent mixtures was higher than for the coherent mixture (one-way RM ANOVA; F(2, 425) = 17.1, p<0.001, Holm-Sidak posthoc test; N = 142). (<b>b</b>) Same experimental protocol as in (a) but odorant <i>A</i> was presented against the background of odorant <i>B</i> (<i>B.A.B</i>) and odorant <i>B</i> against odorant <i>A</i> (<i>A.B.A</i>). Background-odorant lasted 806 ms, starting 6 ms before and stopping 6 ms after the 794-ms long foreground-odorant. The proboscis extension rate for the incoherent mixtures was higher than for the coherent mixture (F(2, 968) = 4.7, p<0.01; N = 323). Experiments in (a) and (b) were done at different times of the year, and the response difference during training and testing to <i>AB</i> might reflect seasonal differences in learning and memory performance. ***, p<0.001; *, p<0.02.</p