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History dependence in insect flight decisions during odor tracking

Pang, Rich and van Breugel, Floris and Dickinson, Michael and Riffell, Jeffrey A. and Fairhall, Adrienne (2018) History dependence in insect flight decisions during odor tracking. PLOS Computational Biology, 14 (2). Art. No. e1005969. ISSN 1553-7358. PMCID PMC5828511. http://resolver.caltech.edu/CaltechAUTHORS:20180221-073540732

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[img] Image (TIFF) (S2 Fig. Positional differences between early and late plume crossings) - Supplemental Material
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[img] Image (TIFF) (S3 Fig. Infotaxis history dependence for varied plume estimate parameters) - Supplemental Material
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[img] Image (TIFF) (S4 Fig. Partial correlation between heading change and crossing number, conditioned on x0 and tflight) - Supplemental Material
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[img] Image (TIFF) (S5 Fig. Effects of varying odor detection threshold on history dependence analysis) - Supplemental Material
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[img] Image (TIFF) (S6 Fig. Distributions of kinematic quantities in base model (before surge-cast or centerline-inferring features were added) vs. empirical data) - Supplemental Material
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[img] Image (TIFF) (S7 Fig. Effects of varying odor detection threshold on hybrid model analysis) - Supplemental Material
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[img] Image (TIFF) (S8 Fig. Position distributions for data and infotaxis results for different wind speeds) - Supplemental Material
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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pcbi.1005969DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5828511/PubMed CentralArticle
https://doi.org/10.1371/journal.pcbi.1005969.s001DOIS1 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s002DOIS2 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s003DOIS3 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s004DOIS4 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s005DOIS5 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s006DOIS6 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s007DOIS7 Fig.
https://doi.org/10.1371/journal.pcbi.1005969.s008DOIS8 Fig.
ORCID:
AuthorORCID
Dickinson, Michael0000-0002-8587-9936
Additional Information:© 2018 Pang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: July 26, 2017; Accepted: January 7, 2018; Published: February 12, 2018. Data Availability Statement: All data files used in this manuscript are publicly available through the Dryad Digital Repository (https://doi.org/10.5061/dryad.n0b8m). Instructions for accessing it through the relevant codebase are given in the code repository landing page on GitHub (https://github.com/rkp8000/wind_tunnel). This work was funded by National Institutes of Health (https://www.nih.gov) grant 5R01DC013693-02 (AF, JAR, MD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have declared that no competing interests exist. Author Contributions: Conceptualization: Rich Pang, Adrienne Fairhall. Data curation: Floris van Breugel, Michael Dickinson. Formal analysis: Rich Pang, Floris van Breugel, Adrienne Fairhall. Funding acquisition: Michael Dickinson, Jeffrey A. Riffell, Adrienne Fairhall. Investigation: Rich Pang, Floris van Breugel, Adrienne Fairhall. Methodology: Rich Pang, Floris van Breugel. Project administration: Rich Pang. Software: Rich Pang. Supervision: Michael Dickinson, Jeffrey A. Riffell, Adrienne Fairhall. Visualization: Rich Pang. Writing ± original draft: Rich Pang. Writing ± review & editing: Rich Pang, Floris van Breugel, Michael Dickinson, Jeffrey A. Riffell, Adrienne Fairhall.
Funders:
Funding AgencyGrant Number
NIH5R01DC013693-02
PubMed Central ID:PMC5828511
Record Number:CaltechAUTHORS:20180221-073540732
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180221-073540732
Official Citation:Pang R, van Breugel F, Dickinson M, Riffell JA, Fairhall A (2018) History dependence in insect flight decisions during odor tracking. PLoS Comput Biol 14(2): e1005969. https://doi.org/10.1371/journal.pcbi.1005969
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:84897
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:22 Feb 2018 18:20
Last Modified:15 Nov 2018 22:54

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