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Nat Neurosci. 2020 Mar 23. doi: 10.1038/s41593-020-0607-9. [Epub ahead of print]

Recurrent architecture for adaptive regulation of learning in the insect brain.

Author information

1
HHMI Janelia Research Campus, Ashburn, VA, USA.
2
Department of Zoology, University of Cambridge, Cambridge, UK.
3
Departments of Neuroscience and Neurology, Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA.
4
Allen Institute for Brain Science, Seattle, WA, USA.
5
Institute of Neurobiology, University of Puerto Rico Medical Science Campus, San Juan, Puerto Rico, USA.
6
Department of Biology, McGill University, Montreal, Quebec, Canada.
7
Department of Genetics, Institute for Biology, University of Leipzig, Leipzig, Germany.
8
Abteilung Genetik von Lernen & Gedächtnis, Leibniz Institut für Neurobiologie, Otto von Guericke University Magdeburg, Institut für Biologie, Verhaltensgenetik, & Center for Behavioral Brain Sciences, Magdeburg, Germany.
9
Department of Biology, University of Washington, Seattle, WA, USA.
10
Department of Neuroscience, Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA. ak3625@columbia.edu.
11
HHMI Janelia Research Campus, Ashburn, VA, USA. acardona@mrc-lmb.cam.ac.uk.
12
MRC Laboratory of Molecular Biology, Cambridge, UK. acardona@mrc-lmb.cam.ac.uk.
13
Department of Physiology, Development & Neuroscience, University of Cambridge, Cambridge, UK. acardona@mrc-lmb.cam.ac.uk.
14
HHMI Janelia Research Campus, Ashburn, VA, USA. mzlatic@mrc-lmb.cam.ac.uk.
15
Department of Zoology, University of Cambridge, Cambridge, UK. mzlatic@mrc-lmb.cam.ac.uk.
16
MRC Laboratory of Molecular Biology, Cambridge, UK. mzlatic@mrc-lmb.cam.ac.uk.

Abstract

Dopaminergic neurons (DANs) drive learning across the animal kingdom, but the upstream circuits that regulate their activity and thereby learning remain poorly understood. We provide a synaptic-resolution connectome of the circuitry upstream of all DANs in a learning center, the mushroom body of Drosophila larva. We discover afferent sensory pathways and a large population of neurons that provide feedback from mushroom body output neurons and link distinct memory systems (aversive and appetitive). We combine this with functional studies of DANs and their presynaptic partners and with comprehensive circuit modeling. We find that DANs compare convergent feedback from aversive and appetitive systems, which enables the computation of integrated predictions that may improve future learning. Computational modeling reveals that the discovered feedback motifs increase model flexibility and performance on learning tasks. Our study provides the most detailed view to date of biological circuit motifs that support associative learning.

PMID:
32203499
DOI:
10.1038/s41593-020-0607-9

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