Alexander Shakeel Bates, Jasper S. Phelps, Minsu Kim, Helen H. Yang, Arie Matsliah, Zaki Ajabi, Eric Perlman, Kevin M. Delgado, Mohammed Abdal Monium Osman, Christopher Salmon, Jay Gager, Benjamin Silverman, Sophia Renauld, Farzaan Salman, Janki Patel, Matthew F. Collie, Jingxuan Fan, Diego A. Pacheco, Yunzhi Zhao, Wenyi Zhang, Laia Serratosa Capdevila, Ruairí J.V. Roberts, Eva J Munnelly, Nina Griggs, Helen Langley, Borja Moya‐Llamas, Zuoyu Zhang, Ryan Maloney, Szi-chieh Yu, Amy Sterling, Marissa Sorek, Krzysztof Kruk, Nikitas Serafetinidis, Serene Dhawan, Finja Klemm, Paul Brooks, Ellen Lesser, Jessica Jones, Sara E Pierce-Lundgren, Su-Yee J. Lee, Yichen Luo, Andrew P. Cook, Theresa H. McKim, Dimitrios Stasi Giakoumas, Benjamin Gorko, Justin Ellis-Joyce, Jiayi Zhang, Emily C. Kophs, Tjalda Falt, Alexa M. Negron-Morales, A Burke, James Hebditch, Kyle Willie, Ryan Willie, S. Yu. Popovych, Nico Kemnitz, Dodam Ih, Kisuk Lee, Ran Lu, Akhilesh Halageri, J. Alexander Bae, Ben Jourdan, Gregory Schwartzman, Damian D Demarest, E.J. Behnke, Doug Bland, Anne Kristiansen, Jaime Skelton, Tom Stocks, Dustin Garner, A.I. Buenfil Hernández, Sandeep Kumar, Jasper S. Phelps, Minsu Kim, Farzaan Salman, Dimitrios Stasi Giakoumas, Benjamin L. de Bivort, Anna Verbe, Gabriel A. Nieves-Sanabria, Devon Jones, Zijin Huang, Sofia Pinto, Celia David, Omaris Y. De Pablo-Crespo, Emily Ye, Wolf Huetteroth, Zequan Liu, Fernando J. Figueroa Santiago, Kevin C. Daly, Sven Dorkenwald, Forrest Collman, Marie P. Suver, Lisa M. Fenk, Michael J. Pankratz, Zepeng Yao, Fei Wang, Stephen J Huston, Tomke Stürner, Gregory S.X.E. Jefferis, Katharina Eichler
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 .