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Nature. 2017 Aug 9;548(7666):175-182. doi: 10.1038/nature23455.

The complete connectome of a learning and memory centre in an insect brain.

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Howard Hughes Medical Institute Janelia Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA.
Department of Biology, University of Konstanz, Universitätsstrasse 10, 78464 Konstanz, Germany.
Mortimer B. Zuckerman Mind Brain Behavior Institute, Department of Neuroscience, Columbia University, 3227 Broadway, New York, New York 10027, USA.
Department of Applied Mathematics and Statistics, Whiting School of Engineering, Johns Hopkins University, 100 Whitehead Hall, 3400 North Charles Street, Baltimore, Maryland 21218, USA.
Abteilung Genetik von Lernen und Gedächtnis, Leibniz Institut für Neurobiologie, 39118 Magdeburg, Germany.
Otto von Guericke Universität Magdeburg, Institut für Biologie, Verhaltensgenetik, Universitätsplatz 2, D-39106 Magdeburg, Germany.
Otto-von-Guericke University Magdeburg, Center for Behavioral Brain Sciences, Universitätsplatz 2, D-39106 Magdeburg, Germany.
Department of Physiology and Cellular Biophysics, Columbia University, Russ Berrie Pavilion, 1150 St Nicholas Avenue, New York, New York 10032, USA.
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.
Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK.


Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higher-order circuit supporting associative memory has not been previously available. Here we reconstruct one such circuit at synaptic resolution, the Drosophila larval mushroom body. We find that most Kenyon cells integrate random combinations of inputs but that a subset receives stereotyped inputs from single projection neurons. This organization maximizes performance of a model output neuron on a stimulus discrimination task. We also report a novel canonical circuit in each mushroom body compartment with previously unidentified connections: reciprocal Kenyon cell to modulatory neuron connections, modulatory neuron to output neuron connections, and a surprisingly high number of recurrent connections between Kenyon cells. Stereotyped connections found between output neurons could enhance the selection of learned behaviours. The complete circuit map of the mushroom body should guide future functional studies of this learning and memory centre.

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