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A lineage-related reciprocal inhibition circuitry for sensory-motor action selection

Benjamin Kottler, Vincenzo G. Fiore, Zoe N. Ludlow, Edgar Buhl, Gerald Vinatier, Richard Faville, Danielle C. Diaper, Alan Stepto, Jonah Dearlove, Yoshitsugu Adachi, Sheena Brown, Chenghao Chen, Daniel A. Solomon, Katherine E. White, Dickon M. Humphrey, Sean M. Buchanan, Stephan J. Sigrist, Keita Endo, Kei Ito, Benjamin de Bivort, Ralf Stanewsky, Raymond J. Dolan, Jean-Rene Martin, James J. L. Hodge, Nicholas J. Strausfeld, Frank Hirth
doi: https://doi.org/10.1101/100420
Benjamin Kottler
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Vincenzo G. Fiore
2Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, UK
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Zoe N. Ludlow
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Edgar Buhl
3University of Bristol, School of Physiology, Pharmacology and Neuroscience, Bristol, UK
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Gerald Vinatier
4CNRS/Université Paris-Sud, Institut des Neurosciences Paris-Saclay (Neuro-PSI), UMR-9197, Gif-sur-Yvette, France
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Richard Faville
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Danielle C. Diaper
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Alan Stepto
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Jonah Dearlove
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Yoshitsugu Adachi
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Sheena Brown
5Department of Neuroscience, University of Arizona, Tucson, Arizona, USA
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Chenghao Chen
6Department of Cell and Developmental Biology, University College London, UK
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Daniel A. Solomon
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Katherine E. White
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Dickon M. Humphrey
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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Sean M. Buchanan
7The Rowland Institute, Center for Brain Science, Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, USA
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Stephan J. Sigrist
8Department of Genetics, Institute for Biology, Free University Berlin, and NeuroCure Cluster of Excellence, Charite, Berlin, Germany
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Keita Endo
9Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan
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Kei Ito
9Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan
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Benjamin de Bivort
7The Rowland Institute, Center for Brain Science, Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, USA
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Ralf Stanewsky
6Department of Cell and Developmental Biology, University College London, UK
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Raymond J. Dolan
2Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, UK
10Max Planck UCL Centre for Computational Psychiatry and Ageing Research, London, UK
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Jean-Rene Martin
4CNRS/Université Paris-Sud, Institut des Neurosciences Paris-Saclay (Neuro-PSI), UMR-9197, Gif-sur-Yvette, France
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James J. L. Hodge
3University of Bristol, School of Physiology, Pharmacology and Neuroscience, Bristol, UK
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Nicholas J. Strausfeld
5Department of Neuroscience, University of Arizona, Tucson, Arizona, USA
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Frank Hirth
1King’s College London, Institute of Psychiatry, Psychology & Neuroscience, Department of Basic & Clinical Neuroscience, London, UK
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  • For correspondence: frank.Hirth@kcl.ac.uk
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ABSTRACT

The insect central complex and vertebrate basal ganglia are forebrain centres involved in selection and maintenance of behavioural actions. However, little is known about the formation of the underlying circuits, or how they integrate sensory information for motor actions. Here, we show that paired embryonic neuroblasts generate central complex ring neurons that mediate sensory-motor transformation and action selection in Drosophila. Lineage analysis resolves four ring neuron subtypes, R1-R4, that form GABAergic inhibition circuitry among inhibitory sister cells. Genetic manipulations, together with functional imaging, demonstrate subtype-specific R neurons mediate the selection and maintenance of behavioural activity. A computational model substantiates genetic and behavioural observations suggesting that R neuron circuitry functions as salience detector using competitive inhibition to amplify, maintain or switch between activity states. The resultant gating mechanism translates facilitation, inhibition and disinhibition of behavioural activity as R neuron functions into selection of motor actions and their organisation into action sequences.

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Posted January 15, 2017.
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A lineage-related reciprocal inhibition circuitry for sensory-motor action selection
Benjamin Kottler, Vincenzo G. Fiore, Zoe N. Ludlow, Edgar Buhl, Gerald Vinatier, Richard Faville, Danielle C. Diaper, Alan Stepto, Jonah Dearlove, Yoshitsugu Adachi, Sheena Brown, Chenghao Chen, Daniel A. Solomon, Katherine E. White, Dickon M. Humphrey, Sean M. Buchanan, Stephan J. Sigrist, Keita Endo, Kei Ito, Benjamin de Bivort, Ralf Stanewsky, Raymond J. Dolan, Jean-Rene Martin, James J. L. Hodge, Nicholas J. Strausfeld, Frank Hirth
bioRxiv 100420; doi: https://doi.org/10.1101/100420
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A lineage-related reciprocal inhibition circuitry for sensory-motor action selection
Benjamin Kottler, Vincenzo G. Fiore, Zoe N. Ludlow, Edgar Buhl, Gerald Vinatier, Richard Faville, Danielle C. Diaper, Alan Stepto, Jonah Dearlove, Yoshitsugu Adachi, Sheena Brown, Chenghao Chen, Daniel A. Solomon, Katherine E. White, Dickon M. Humphrey, Sean M. Buchanan, Stephan J. Sigrist, Keita Endo, Kei Ito, Benjamin de Bivort, Ralf Stanewsky, Raymond J. Dolan, Jean-Rene Martin, James J. L. Hodge, Nicholas J. Strausfeld, Frank Hirth
bioRxiv 100420; doi: https://doi.org/10.1101/100420

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