1. History dependence in insect flight decisions during odor tracking
- Author
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Michael H. Dickinson, Floris van Breugel, Richard Pang, Adrienne L. Fairhall, and Jeffrey A. Riffell
- Subjects
0301 basic medicine ,Atmospheric Science ,Physiology ,Wind ,Disease Vectors ,Animal flight ,Tracking (particle physics) ,Mosquitoes ,Sexual Behavior, Animal ,0302 clinical medicine ,Aedes ,Medicine and Health Sciences ,lcsh:QH301-705.5 ,Mathematics ,Behavior, Animal ,Ecology ,Organic Compounds ,Drosophila Melanogaster ,Eukaryota ,Contrast (statistics) ,Animal Models ,Plume ,Insects ,Smell ,Chemistry ,Variable (computer science) ,Infectious Diseases ,Memory, Short-Term ,Experimental Organism Systems ,Computational Theory and Mathematics ,Modeling and Simulation ,Physical Sciences ,Drosophila ,Biological system ,Flight (Biology) ,Algorithms ,Research Article ,Arthropoda ,Decision Making ,Research and Analysis Methods ,Models, Biological ,Insect flight ,03 medical and health sciences ,Cellular and Molecular Neuroscience ,Meteorology ,Model Organisms ,Genetics ,Animals ,Learning ,Computer Simulation ,Information gain ,Molecular Biology ,Ecology, Evolution, Behavior and Systematics ,Probability ,Ethanol ,Biological Locomotion ,Organic Chemistry ,Organisms ,Chemical Compounds ,Biology and Life Sciences ,Invertebrates ,Insect Vectors ,Species Interactions ,030104 developmental biology ,Odor ,lcsh:Biology (General) ,Alcohols ,Flight, Animal ,Odorants ,Earth Sciences ,Linear Models ,Insect Flight ,030217 neurology & neurosurgery - Abstract
Natural decision-making often involves extended decision sequences in response to variable stimuli with complex structure. As an example, many animals follow odor plumes to locate food sources or mates, but turbulence breaks up the advected odor signal into intermittent filaments and puffs. This scenario provides an opportunity to ask how animals use sparse, instantaneous, and stochastic signal encounters to generate goal-oriented behavioral sequences. Here we examined the trajectories of flying fruit flies (Drosophila melanogaster) and mosquitoes (Aedes aegypti) navigating in controlled plumes of attractive odorants. While it is known that mean odor-triggered flight responses are dominated by upwind turns, individual responses are highly variable. We asked whether deviations from mean responses depended on specific features of odor encounters, and found that odor-triggered turns were slightly but significantly modulated by two features of odor encounters. First, encounters with higher concentrations triggered stronger upwind turns. Second, encounters occurring later in a sequence triggered weaker upwind turns. To contextualize the latter history dependence theoretically, we examined trajectories simulated from three normative tracking strategies. We found that neither a purely reactive strategy nor a strategy in which the tracker learned the plume centerline over time captured the observed history dependence. In contrast, “infotaxis”, in which flight decisions maximized expected information gain about source location, exhibited a history dependence aligned in sign with the data, though much larger in magnitude. These findings suggest that while true plume tracking is dominated by a reactive odor response it might also involve a history-dependent modulation of responses consistent with the accumulation of information about a source over multi-encounter timescales. This suggests that short-term memory processes modulating decision sequences may play a role in natural plume tracking., Author summary Many important behaviors require animals to make extended decision sequences in response to complex stimuli. In this study we investigated the sequences of navigational decisions made by fruit flies and mosquitoes while tracking odor plumes, which are generally subject to turbulence. By examining video-taped 3D trajectories of these insects flying in a wind tunnel containing an attractive odor plume, we asked what features of encounters with the plume influenced odor-triggered flight decisions. Most notably, we found that although the average response was dominated by a reflexive upwind turn, its strength was modulated by the history of prior plume encounters throughout the trajectory. While no theoretical strategy we simulated captured all aspects of the data, the algebraic sign of the history dependence was only recapitulated in a model where a simulated tracking agent maximizes information about the position of the plume source. This suggests that real odor tracking may involve short-term memory processes over multi-encounter timescales that are consistent with the accumulation of information about source location.
- Published
- 2018