An internal expectation guides Drosophila egg-laying decisions
Abstract
To better understand how animals make ethologically relevant decisions, we studied egg-laying substrate choice in Drosophila . We found that flies dynamically increase or decrease their egg-laying rates while exploring substrates so as to target eggs to the best, recently visited option. Visiting the best option typically yielded inhibition of egg laying on other substrates for many minutes. Our data support a model in which flies compare the current substrate's value with an internally constructed expectation on the value of available options to regulate the likelihood of laying an egg. We show that dopamine neuron activity is critical for learning and/or expressing this expectation, similar to its role in certain tasks in vertebrates. Integrating sensory experiences over minutes to generate an estimate of the quality of available options allows flies to use a dynamic reference point for judging the current substrate and might be a general way in which decisions are made.
Copyright and License
Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).
Acknowledgement
We thank the Rockefeller University Precision Instrumentation Technologies facility for access to fabrication equipment; the Bloomington Drosophila Stock Center (NIH P400D018537), L. Zhao, S. Durkin, W. Li, N. Yapici, J. Tuthill, K. Kuan, M. Wu, and V. Ruta for fly stocks; A. Adachi for help immunostaining many of the screened lines; N. Rangarajan, S. Cohen, and S. Durkin for assistance with experiments; V. Ruta and I. Morantte for discussions regarding dopamine receptor mutants; T. Mohren for ideas regarding modeling; and the reviewers for helpful comments, particularly reviewer #1 for posing the insightful model in fig. S4 (C and D).
Funding
Research reported in this publication was supported by a Brain Initiative grant from the National Institute of Neurological Disorders and Stroke (NIH R01NS121904) and a New Innovator grant from the National Institute of Drug Abuse (NIH DP2DA035148) to G.M. alongside a Leon Levy Foundation fellowship and a Kavli Neural Systems Institute grant to V.V. G.M. is a Howard Hughes Medical Institute Investigator.
Contributions
V.V. and G.M. conceived the initial study and wrote the manuscript. V.V., with input from G.M., designed the experiments, performed the experiments, analyzed the data, interpreted the results, and decided on new experiments. Z.W., V.C., A.C., R.L., and S.L.S. assisted with performing various egg-laying experiments and interpreting the results. H.A. developed code to markedly speed up manual annotation of egg deposition events and provided feedback on modeling.
Data Availability
All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. All fly tracking data used in the paper are available on the DANDI Archive (ID: 000212; https://dandiarchive.org/dandiset/000212).
Supplemental Material
Tables S1 and S2.
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Additional details
- National Institute of Neurological Disorders and Stroke
- NIH R01NS121904
- National Institute on Drug Abuse
- NIH DP2DA035148
- Leon Levy Foundation
- Fellowship -
- Rockefeller University
- Kavli Neural Systems Institute -
- Howard Hughes Medical Institute
- Investigator -
- Accepted
-
2022-09-14Accepted
- Caltech groups
- Division of Biology and Biological Engineering
- Publication Status
- Published