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Distributed control circuits across a brain-and-cord connectome
Alexander Shakeel Bates (Harvard University, University of Oxford), Jasper S. Phelps (Harvard University, École Polytechnique Fédérale de Lausanne), Minsu Kim (Harvard University), Helen H. Yang (Harvard University), Arie Matsliah (Princeton University), Zaki Ajabi (Harvard University), Eric Perlman, Kevin M. Delgado (Harvard University), Mohammed Abdal Monium Osman (Harvard University), Christopher K. Salmon (Princeton University), Jay Gager (Princeton University), Benjamin Silverman (Princeton University), Sophia Renauld (Harvard University), Farzaan Salman (West Virginia University, Harvard University), Janki Patel (Harvard University), Matthew F. Collie (Harvard University), Jingxuan Fan (Harvard University), Diego A. Pacheco (Harvard University), Yunzhi Zhao (Harvard University), Wenyi Zhang (Harvard University), Laia Serratosa Capdevila, Ruairí J.V. Roberts, Eva J Munnelly, Nina Griggs, Helen Langley, Borja Moya‐Llamas (Harvard University, Colorado College), Zuoyu Zhang (Chinese Academy of Medical Sciences & Peking Union Medical College, Princeton University), Ryan T. Maloney (Harvard University, Colorado College), Szi-chieh Yu (Princeton University), Amy Robinson Sterling (Princeton University), Marissa Sorek (Princeton University), Krzysztof Kruk (Princeton University), Nikitas Serafetinidis (MRC Laboratory of Molecular Biology), Serene Dhawan (Princeton University, Leipzig University), Finja Klemm (University of Cambridge, Leipzig University), Paul S Brooks (University of Cambridge, University of Chicago), Ellen Lesser (University of Washington, University of Chicago), Jessica M. Jones (University of Washington), Sara E. Pierce-Lundgren (University of Washington), Su-Yee J. Lee (University of Washington), Yichen Luo (West Virginia University, University of Washington), Andrew P. Cook (University of Nevada, Reno, Virginia Tech), Theresa H. McKim (University of Nevada, Reno, Vanderbilt University), Dimitrios Stasi Giakoumas (University of Iowa, University of Florida), Benjamin Gorko (University of California, Santa Barbara, University of Puerto Rico, Medical Sciences Campus), Justin Ellis-Joyce (Howard Hughes Medical Institute, Johns Hopkins University), Jiayi Zhang (Chinese Academy of Sciences, Princeton University), Emily C. Kophs (Vanderbilt University, Princeton University), Tjalda Falt (Princeton University, Max Planck Institute for Biological Intelligence), Alexa M. Negron-Morales (University of Puerto Rico, Medical Sciences Campus), A Burke (Princeton University), James Hebditch (Princeton University), Kyle Patrick Willie (Princeton University), Ryan Willie (Princeton University), Sergiy Popovych, Nico Kemnitz, Dodam Ih (University of Edinburgh), Kisuk Lee (Japan Advanced Institute of Science and Technology), Ran Lu (University of Bonn), Akhilesh Halageri (Princeton University), J. Alexander Bae, Ben Jourdan (University of Edinburgh), Gregory Schwartzman (Japan Advanced Institute of Science and Technology), Damian D. Demarest (University of Bonn), Emily Behnke (Princeton University), Doug Bland (West Virginia University, Harvard University), Anne Kristiansen (West Virginia University), Jaime Skelton, Tom Stocks (Princeton University), Dustin Garner (Allen Institute for Brain Science, University of California, Santa Barbara), Anthony Hernandez (Allen Institute for Brain Science), Sandeep Kumar (Vanderbilt University, Princeton University), Jasper S. Phelps (Harvard University, Max Planck Institute for Biological Intelligence), Minsu Kim (University of Bonn, Harvard University), Farzaan Salman (West Virginia University, Harvard University), Dimitrios Stasi Giakoumas (University of Iowa, University of Florida), Benjamin L. de Bivort (Harvard University, University of Puerto Rico, Medical Sciences Campus), Anna Verbe (University of Puerto Rico, Medical Sciences Campus, Princeton University), Gabriel A. Nieves-Sanabria (University of Puerto Rico, Medical Sciences Campus, Virginia Tech), Devon L. Jones (University of Nevada, Reno, University of Würzburg), Zijin Huang (Princeton University), Sofia Pinto (Champalimaud Foundation, Howard Hughes Medical Institute), Celia David (Howard Hughes Medical Institute), Omaris Y. De Pablo-Crespo (University of Puerto Rico, Medical Sciences Campus, University of Washington), Emily Ye (Harvard University, University of Washington), Wolf Huetteroth (Princeton University, Leipzig University), Zequan Liu (Harvard University, RWTH Aachen University), Fernando J. Figueroa Santiago (University of Puerto Rico, Medical Sciences Campus, Princeton University), Kevin C. Daly (West Virginia University, Harvard University), Sven Dorkenwald (Allen Institute for Brain Science, Harvard University), Forrest Collman (Boston Children's Hospital, Allen Institute for Brain Science), Marie P. Suver (Vanderbilt University), Lisa M. Fenk (Max Planck Institute for Biological Intelligence), Michael J. Pankratz (University of Bonn), Zepeng Yao (University of Florida), Fei Wang (Chinese Academy of Sciences, Center for Excellence in Brain Science and Intelligence Technology), Stephen J Huston (Columbia University), Tomke Stürner (MRC Laboratory of Molecular Biology), Gregory S.X.E. Jefferis (MRC Laboratory of Molecular Biology, University of Cambridge), Katharina Eichler (Leipzig University), Andrew Michael Seeds (University of Puerto Rico, Medical Sciences Campus), Stefanie Hampel (University of Puerto Rico, Medical Sciences Campus), Sweta Agrawal (Virginia Tech), Tatsuo S. Okubo (Chinese Academy of Medical Sciences & Peking Union Medical College, Chinese Institute for Brain Research), Meet Zandawala (University of Nevada, Reno, University of Würzburg), Thomas Macrina, Diane-Yayra Adjavon (Howard Hughes Medical Institute), Jan Funke (Howard Hughes Medical Institute), John C Tuthill (University of Washington), Anthony W. Azevedo (University of Washington), H. Sebastian Seung (Princeton University), Benjamin L. de Bivort (Harvard University), Mala Murthy (Princeton University), Jan Drugowitsch (Harvard University), Rachel I. Wilson (Harvard University), Wei-Chung Allen Lee (Boston Children's Hospital, Harvard University)
Résumé : Abstract Just as genomes revolutionized molecular genetics, connectomes (maps of neurons and synapses) are transforming neuroscience. To date, the only organisms with complete connectomes are worms 1–3 , sea squirts 4 and comb jellies 5 (10 3 –10 4 synapses). By contrast, the fruit fly is more complex (10 8 synaptic connections), with a brain that supports learning and spatial memory 6,7 and an intricate ventral nerve cord analogous to the vertebrate spinal cord 8–12 . Here we report a densely reconstructed adult fly connectome that unites the brain and ventral nerve cord, and we leverage this resource to investigate principles of neural control. We show that effector neurons (motor neurons, endocrine cells and efferent neurons targeting the viscera) are primarily influenced by sensory neurons in the same body part, forming local feedback loops. These local loops are linked by long-range circuits that involve ascending and descending neurons organized into behaviour-centric modules. Single ascending and descending neurons are often positioned to influence the voluntary movements of multiple body parts, together with the endocrine cells or visceral organs that support those movements. Brain regions involved in learning and navigation supervise these circuits. These results reveal an architecture that is distributed, parallelized and embodied, reminiscent of distributed control architectures in engineered systems 13,14 .