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Neuron. 2019 Nov 6;104(3):544-558.e6. doi: 10.1016/j.neuron.2019.07.028. Epub 2019 Aug 27.

A Neural Circuit Arbitrates between Persistence and Withdrawal in Hungry Drosophila.

Author information

1
Technical University of Munich, School of Life Sciences, 85354 Freising, Germany.
2
Technical University of Munich, School of Life Sciences, 85354 Freising, Germany; Max Planck Institute for Brain Research, Computation in Neural Circuits Group, 60438 Frankfurt, Germany.
3
Max Planck Institute of Neurobiology, Chemosensory Coding Group, 82152 Martinsried, Germany.
4
Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
5
HHMI Janelia Research Campus, Ashburn, VA 20147, USA.
6
Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK; Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK.
7
Technical University of Munich, School of Life Sciences, 85354 Freising, Germany; ZIEL - Institute for food and health, 85354 Freising, Germany; Max Planck Institute of Neurobiology, Chemosensory Coding Group, 82152 Martinsried, Germany. Electronic address: ilona.grunwald@tum.de.

Abstract

In pursuit of food, hungry animals mobilize significant energy resources and overcome exhaustion and fear. How need and motivation control the decision to continue or change behavior is not understood. Using a single fly treadmill, we show that hungry flies persistently track a food odor and increase their effort over repeated trials in the absence of reward suggesting that need dominates negative experience. We further show that odor tracking is regulated by two mushroom body output neurons (MBONs) connecting the MB to the lateral horn. These MBONs, together with dopaminergic neurons and Dop1R2 signaling, control behavioral persistence. Conversely, an octopaminergic neuron, VPM4, which directly innervates one of the MBONs, acts as a brake on odor tracking by connecting feeding and olfaction. Together, our data suggest a function for the MB in internal state-dependent expression of behavior that can be suppressed by external inputs conveying a competing behavioral drive.

KEYWORDS:

DopR2; Drosophila melanogaster; dopamine; foraging; goal-directed behavior; learning; mushroom body; octopamine; olfactory system; persistence

PMID:
31471123
DOI:
10.1016/j.neuron.2019.07.028
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