RESUMO
Odour plumes in the wild are spatially complex and rapidly fluctuating structures carried by turbulent airflows1-4. To successfully navigate plumes in search of food and mates, insects must extract and integrate multiple features of the odour signal, including odour identity5, intensity6 and timing6-12. Effective navigation requires balancing these multiple streams of olfactory information and integrating them with other sensory inputs, including mechanosensory and visual cues9,12,13. Studies dating back a century have indicated that, of these many sensory inputs, the wind provides the main directional cue in turbulent plumes, leading to the longstanding model of insect odour navigation as odour-elicited upwind motion6,8-12,14,15. Here we show that Drosophila melanogaster shape their navigational decisions using an additional directional cue-the direction of motion of odours-which they detect using temporal correlations in the odour signal between their two antennae. Using a high-resolution virtual-reality paradigm to deliver spatiotemporally complex fictive odours to freely walking flies, we demonstrate that such odour-direction sensing involves algorithms analogous to those in visual-direction sensing16. Combining simulations, theory and experiments, we show that odour motion contains valuable directional information that is absent from the airflow alone, and that both Drosophila and virtual agents are aided by that information in navigating naturalistic plumes. The generality of our findings suggests that odour-direction sensing may exist throughout the animal kingdom and could improve olfactory robot navigation in uncertain environments.
Assuntos
Drosophila melanogaster , Percepção de Movimento , Odorantes , Percepção Olfatória , Navegação Espacial , Vento , Animais , Drosophila melanogaster/anatomia & histologia , Drosophila melanogaster/fisiologia , Odorantes/análise , Navegação Espacial/fisiologia , Percepção de Movimento/fisiologia , Fatores de Tempo , Percepção Olfatória/fisiologia , Antenas de Artrópodes/fisiologia , Sinais (Psicologia) , Caminhada/fisiologiaRESUMO
In aquatic and terrestrial environments, odorants are dispersed by currents that create concentration distributions that are spatially and temporally complex. Animals navigating in a plume must therefore rely upon intermittent, and time-varying information to find the source. Navigation has typically been studied as a spatial information problem, with the aim of movement towards higher mean concentrations. However, this spatial information alone, without information of the temporal dynamics of the plume, is insufficient to explain the accuracy and speed of many animals tracking odors. Recent studies have identified a subpopulation of olfactory receptor neurons (ORNs) that consist of intrinsically rhythmically active 'bursting' ORNs (bORNs) in the lobster, Panulirus argus. As a population, bORNs provide a neural mechanism dedicated to encoding the time between odor encounters. Using a numerical simulation of a large-scale plume, the lobster is used as a framework to construct a computer model to examine the utility of intermittency for orienting within a plume. Results show that plume intermittency is reliably detectable when sampling simulated odorants on the order of seconds, and provides the most information when animals search along the plume edge. Both the temporal and spatial variation in intermittency is predictably structured on scales relevant for a searching animal that encodes olfactory information utilizing bORNs, and therefore is suitable and useful as a navigational cue.