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History dependence in insect flight decisions during odor tracking.

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.

SUBMITTER: Pang R

PROVIDER: S-EPMC5828511 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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History dependence in insect flight decisions during odor tracking.

Pang Rich R van Breugel Floris F Dickinson Michael M Riffell Jeffrey A JA Fairhall Adrienne A

PLoS computational biology 20180212 2

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 ...[more]

PMID: 29432454

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Project description:Insects are model systems for swarming robotic agents, yet engineered descriptions do not fully explain the mechanisms by which they provide onboard sensing and feedback to support such motions; in particular, the exact value and population distribution of visuomotor processing delays are not yet quantified, nor the effect of such delays on a visually-interconnected swarm. This study measures untethered insects performing a solo in-flight visual tracking task and applies system identification techniques to build an experimentally-consistent model of the visual tracking behaviors, and then integrates the measured experimental delay and its variation into a visually interconnected swarm model to develop theoretical and simulated solutions and stability limits. The experimental techniques include the development of a moving visual stimulus and real-time multi camera based tracking system called VISIONS (Visual Input System Identification from Outputs of Naturalistic Swarms) providing the capability to recognize and simultaneously track both a visual stimulus (input) and an insect at a frame rate of 60-120 Hz. A frequency domain analysis of honeybee tracking trajectories is conducted via fast Fourier and Chirp Z transforms, identifying a coherent linear region and its model structure. The model output is compared in time and frequency domain simulations. The experimentally measured delays are then related to probability density functions, and both the measured delays and their distribution are incorporated as inter-agent interaction delays in a second order swarming dynamics model. Linear stability and bifurcation analysis on the long range asymptotic behavior is used to identify delay distributions leading to a family of solutions with stable and unstable swarm center of mass (barycenter) locations. Numerical simulations are used to verify these results with both continuous and measured distributions. The results of this experiment quantify a model structure and temporal lag (transport delay) in the closed loop dynamics, and show that this delay varies across 50 individuals from 5-110ms, with an average delay of 22ms and a standard deviation of 40ms. When analyzed within the swarm model, the measured delays support a diversity of solutions and indicate an unstable barycenter.

Dataset Information

History dependence in insect flight decisions during odor tracking.

Publications

History dependence in insect flight decisions during odor tracking.

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