Distributed control circuits across a brain-and-cord connectome

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Abstract
Just as genomes revolutionized molecular genetics, connectomes (maps of neurons and synapses) are transforming neuroscience. To date, the only species with complete connectomes are worms 1-3 and sea squirts4 (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 5,6 and an intricate ventral nerve cord analogous to the vertebrate spinal cord 7-11 . Here we report the first 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 involving ascending and descending neurons organized into behavior-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 12,13 .
Funding Information
  • National Institutes of Health (R01NS121874)
  • National Institutes of Health (RF1MH117808)
  • National Institutes of Health (U24NS126935)
  • National Institutes of Health (RF1MH117815)
  • National Institutes of Health (U19NS118246)
  • National Institutes of Health (K99NS129759)
  • National Institutes of Health (R00NS117657)
  • National Institutes of Health (R01NS102333)
  • National Institutes of Health (RF1NS128785)
  • National Institutes of Health (UM1NS132253)
  • National Institutes of Health (U24NS139927)
  • National Institutes of Health (RF1MH128840)
  • National Institutes of Health (R01NS121911)
  • National Institutes of Health (U01NS131438)
  • National Institutes of Health (T32GM144273)
  • Howard Hughes Medical Institute (PJ100000343)
  • Howard Hughes Medical Institute (GT15790)
  • Howard Hughes Medical Institute (HHMI Investigator)
  • New York Stem Cell Foundation (Robertson Neuroscience Investigator Award)
  • Deutsche Forschungsgemeinschaft (ZA1296/1-1)
  • Deutsche Forschungsgemeinschaft (EXC2151-390873048)
  • Deutsche Forschungsgemeinschaft (PA787/7-3)
  • Deutsche Forschungsgemeinschaft (PA787/9-3)
  • NV INBRE (GM103440)
  • Japan Society for the Promotion of Science (KAKENHI 25K00370)
  • Japan Science and Technology Agency (ASPIRE JPMJAP2302)
  • Japan Science and Technology Agency (CRONOS JPMJCS24K2)
  • Shanahan Family Foundation
  • Kempner Institute for the Study of Natural and Artificial Intelligence
  • Alice and Joseph Brooks Fund

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