Circuits for integrating learned and innate valences in the insect brain
- University of Cambridge, United Kingdom
- Columbia University, Zuckerman Institute, United States
- Howard Hughes Medical Institute, United States
- University of Puerto Rico Medical Sciences Campus, Puerto Rico
- New York University, United States
- Harvard University, United States
- University of California, United States
- MRC Laboratory of Molecular Biology, United Kingdom
Abstract
Animal behavior is shaped both by evolution and by individual experience. Parallel brain pathways encode innate and learned valences of cues, but the way in which they are integrated during action-selection is not well understood. We used electron microscopy to comprehensively map with synaptic resolution all neurons downstream of all Mushroom Body output neurons (encoding learned valences) and characterized their patterns of interaction with Lateral Horn neurons (encoding innate valences) in Drosophila larva. The connectome revealed multiple convergence neuron types that receive convergent Mushroom Body and Lateral Horn inputs. A subset of these receives excitatory input from positive-valence MB and LH pathways and inhibitory input from negative-valence MB pathways. We confirmed functional connectivity from LH and MB pathways and behavioral roles of two of these neurons. These neurons encode integrated odor value and bidirectionally regulate turning. Based on this we speculate that learning could potentially skew the balance of excitation and inhibition onto these neurons and thereby modulate turning. Together, our study provides insights into the circuits that integrate learned and innate valences to modify behavior.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files are provided for Figures 2 to 6.
Article and author information
Author details
Benjamin T Cocanougher
Gregory SXE Jefferis
Aravinthan DT Samuel
Funding
Howard Hughes Medical Institute
- Claire Eschbach
- Akira Fushiki
- Michael Winding
- Bruno Afonso
- Ingrid V Andrade
- Benjamin T Cocanougher
- Javier Valdes-Aleman
- James W Truman
- Albert Cardona
- Marta Zlatic
European Research Council (RG95162)
- Claire Eschbach
- Michael Winding
- Marta Zlatic
Wellcome Trust (RG86459)
- Marta Zlatic
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India
Version history
- Preprint posted: April 24, 2020 (view preprint)
- Received: September 30, 2020
- Accepted: November 3, 2021
- Accepted Manuscript published: November 10, 2021 (version 1)
- Accepted Manuscript updated: November 11, 2021 (version 2)
- Version of Record published: November 25, 2021 (version 3)
Copyright
© 2021, Eschbach et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Circuits for integrating learned and innate valences in the insect brain
eLife 10:e62567.
https://doi.org/10.7554/eLife.62567
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