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Synaptic combinatorial molecular mechanisms generate repertoires of innate and learned behavior

Noboru H. Komiyama, Louie N. van de Lagemaat, Lianne E. Stanford, Charles M. Pettit, Douglas J. Strathdee, Karen E. Strathdee, David G. Fricker, Eleanor J. Tuck, Kathryn A. Elsegood, Tomás J. Ryan, Jess Nithianantharajah, Nathan G. Skene, Mike D. R. Croning, View ORCID ProfileSeth G. N. Grant
doi: https://doi.org/10.1101/500389
Noboru H. Komiyama
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Louie N. van de Lagemaat
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Lianne E. Stanford
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Charles M. Pettit
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Douglas J. Strathdee
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
3Cancer Research UK Beatson Institute, Garscube Estate, Glasgow, G61 1BD, UK
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Karen E. Strathdee
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
4Wolfson Wohl Cancer Research Centre, University of Glasgow, Switchback Road, Glasgow G61 1QH, UK
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David G. Fricker
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Eleanor J. Tuck
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Kathryn A. Elsegood
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Tomás J. Ryan
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
5Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland
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Jess Nithianantharajah
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
6Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, 3052, Victoria, Australia
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Nathan G. Skene
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Mike D. R. Croning
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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Seth G. N. Grant
1Genes to Cognition Programme, Centre for Clinical Brain Sciences, Chancellor’s Building, University of Edinburgh, Edinburgh, EH16 4SB, UK
2Genes to Cognition Programme, The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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  • ORCID record for Seth G. N. Grant
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Abstract

Although molecular mechanisms underpinning specific behaviors have been described, whether there are mechanisms that orchestrate a behavioral repertoire is unknown. To test if the postsynaptic proteome of excitatory synapses could impart such a mechanism we conducted the largest genetic study of mammalian synapses yet undertaken. A repertoire of sixteen innate and learned behaviors was assessed from 290,850 measures in 55 lines of mutant mice carrying targeted mutations in the principal classes of postsynaptic proteins. Each innate and learned behavior used a different combination of proteins. These combinations were comprised of proteins that amplified or attenuated the magnitude of each behavioral response. All behaviors required proteins found in PSD95 supercomplexes. We show the vertebrate increase in proteome complexity drove an expansion in behavioral repertoires and generated susceptibility to a wide range of diseases. Our results reveal a molecular mechanism that generates a versatile and complex behavioral repertoire that is central to human behavioral disorders.

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Posted December 19, 2018.
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Synaptic combinatorial molecular mechanisms generate repertoires of innate and learned behavior
Noboru H. Komiyama, Louie N. van de Lagemaat, Lianne E. Stanford, Charles M. Pettit, Douglas J. Strathdee, Karen E. Strathdee, David G. Fricker, Eleanor J. Tuck, Kathryn A. Elsegood, Tomás J. Ryan, Jess Nithianantharajah, Nathan G. Skene, Mike D. R. Croning, Seth G. N. Grant
bioRxiv 500389; doi: https://doi.org/10.1101/500389
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Synaptic combinatorial molecular mechanisms generate repertoires of innate and learned behavior
Noboru H. Komiyama, Louie N. van de Lagemaat, Lianne E. Stanford, Charles M. Pettit, Douglas J. Strathdee, Karen E. Strathdee, David G. Fricker, Eleanor J. Tuck, Kathryn A. Elsegood, Tomás J. Ryan, Jess Nithianantharajah, Nathan G. Skene, Mike D. R. Croning, Seth G. N. Grant
bioRxiv 500389; doi: https://doi.org/10.1101/500389

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