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A neural circuit arbitrates between perseverance and withdrawal in hungry Drosophila

S. Sayin, J.-F. De Backer, M.E. Wosniack, L.P. Lewis, K.P. Siju, L.-M. Frisch, P. Schlegel, A. Edmondson-Stait, N. Sharifi, C.B. Fisher, S. Calle-Schuler, S. Lauritzen, D.D. Bock, M. Costa, G.S.X.E. Jefferis, J. Gjorgjieva, I.C. Grunwald Kadow
doi: https://doi.org/10.1101/259119
S. Sayin
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
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J.-F. De Backer
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
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M.E. Wosniack
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
4Max Planck Institute for Brain Research, Max-von-Laue-Str. 4, 60438 Frankfurt, Germany
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L.P. Lewis
3Max Planck Institute of Neurobiology, Am Klopferspitz 18, 82152 Martinsried, Germany
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K.P. Siju
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
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L.-M. Frisch
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
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P. Schlegel
5Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
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A. Edmondson-Stait
5Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
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N. Sharifi
6HHMI Janelia Research Campus, Ashburn, VA 20147, USA
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C.B. Fisher
6HHMI Janelia Research Campus, Ashburn, VA 20147, USA
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S. Calle-Schuler
6HHMI Janelia Research Campus, Ashburn, VA 20147, USA
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S. Lauritzen
6HHMI Janelia Research Campus, Ashburn, VA 20147, USA
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D.D. Bock
6HHMI Janelia Research Campus, Ashburn, VA 20147, USA
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M. Costa
5Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
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G.S.X.E. Jefferis
5Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
7Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK
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J. Gjorgjieva
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
4Max Planck Institute for Brain Research, Max-von-Laue-Str. 4, 60438 Frankfurt, Germany
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I.C. Grunwald Kadow
1Technical University of Munich, School of Life Sciences, Liesel-Beckmann-Str. 4, 85354 Freising, Germany
2ZIEL - Institute for food and health, Weihenstephaner Berg 1, 85354 Freising, Germany
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Abstract

In pursuit of palatable food, hungry animals mobilize significant energy resources and overcome obstacles, exhaustion and fear. Their perseverance depends on metabolic state, internal motivation and the expected benefit. Sustained commitment to a trying task is crucial, however, disengagement from one behavior to engage into another can be essential for optimal adaptation and survival. How neural circuits allow prioritizing perseverance over withdrawal based on the animal’s need is not understood. Using a single fly spherical treadmill, we show that hungry flies display increasing perseverance to track a food odor in the repeated absence of the predicted food reward. While this perseverance is mediated by a group of dopaminergic neurons, a subset of neurons expressing octopamine, the invertebrate counterpart of noradrenaline, provide reward feedback and counteract dopamine-motivated food seeking. Our data and modeling suggest that two important neuromodulators tally internal and external signals to coordinate motivation-dependent antagonistic behavioral drives: perseverance vs. change of behavior.

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  • Lack of reward stimulates perseverance, and not quitting.

  • Dopaminergic neurons previously implicated in aversive learning promote perseverance.

  • Sugar responsive octopaminergic neurons directly counteract perseverant odor tracking through a downstream inhibitory neuron.

  • Computational modeling supports a simple neural circuit featuring antagonistic functions for dopamine and octopamine as tallies of expense and gain.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted February 19, 2018.
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A neural circuit arbitrates between perseverance and withdrawal in hungry Drosophila
S. Sayin, J.-F. De Backer, M.E. Wosniack, L.P. Lewis, K.P. Siju, L.-M. Frisch, P. Schlegel, A. Edmondson-Stait, N. Sharifi, C.B. Fisher, S. Calle-Schuler, S. Lauritzen, D.D. Bock, M. Costa, G.S.X.E. Jefferis, J. Gjorgjieva, I.C. Grunwald Kadow
bioRxiv 259119; doi: https://doi.org/10.1101/259119
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A neural circuit arbitrates between perseverance and withdrawal in hungry Drosophila
S. Sayin, J.-F. De Backer, M.E. Wosniack, L.P. Lewis, K.P. Siju, L.-M. Frisch, P. Schlegel, A. Edmondson-Stait, N. Sharifi, C.B. Fisher, S. Calle-Schuler, S. Lauritzen, D.D. Bock, M. Costa, G.S.X.E. Jefferis, J. Gjorgjieva, I.C. Grunwald Kadow
bioRxiv 259119; doi: https://doi.org/10.1101/259119

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