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Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higherorder circuit supporting associative memory has not been previously available. We reconstructed one such circuit at synaptic resolution, the Drosophila larval mushroom body, and found that most Kenyon cells integrate random combinations of inputs but a subset receives stereotyped inputs from single projection neurons. This organization maximizes performance of a model output neuron on a stimulus discrimination task. We also report a novel canonical circuit in each mushroom body compartment with previously unidentified connections: reciprocal Kenyon cell to modulatory neuron connections, modulatory neuron to output neuron connections, and a surprisingly high number of recurrent connections between Kenyon cells. Stereotyped connections between output neurons could enhance the selection of learned responses. The complete circuit map of the mushroom body should guide future functional studies of this learning and memory center.Massively parallel, higher-order neuronal circuits such as the cerebellum and insect mushroom body serve to form and retain associations between stimuli and reinforcement in vertebrates and higher invertebrates [1][2][3][4][5][6] . Although these systems provide a biological substrate for adaptive behavior, no complete synapseresolution wiring diagram of their connectivity has been available to guide analysis and inspire understanding. The mushroom body (MB) is a higher-order parallel fiber system in many invertebrate brains, including hemimetabolous as well as holometabolous insects and their larval stages 6 . MB function is essential for associative learning in adult insects 1;3-5 and in Drosophila larvae 1;7;8 , from the earliest larval stages onward 9 . Indeed, the basic organization of the adult and the larval MB and their afferent circuits is very similar; however, larvae have about an order of magnitude fewer neurons 7 . Thus, to systematically investigate the organizational logic of the MB, we used serial section electron microscopy (EM) to map with synaptic resolution the complete MB connectome in a first instar Drosophila larva (L1; Fig. 1a). L1 are foraging animals capable of all behaviors previously described in later larval stages 10 , including adaptive behaviors dependent on associative learning 7;9 (Fig. 1b). Their smaller neurons enable fast EM imaging of the entire nervous system and reconstruction of complete circuits 11;12 . Models of sensory processing in many neural circuits feature neurons that fire in response to combinations of sensory inputs, generating a high-dimensional representation of the sensory environment 13 . The intrinsic MB neurons, the Kenyon cells (KCs), integrate in their dendrites inputs from combinations of projection neurons (PNs) that encode various stimuli, predominantly olfactory in both adult 1;4-6 , and larva 12;14 , but also thermal, gustatory
Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higherorder circuit supporting associative memory has not been previously available. We reconstructed one such circuit at synaptic resolution, the Drosophila larval mushroom body, and found that most Kenyon cells integrate random combinations of inputs but a subset receives stereotyped inputs from single projection neurons. This organization maximizes performance of a model output neuron on a stimulus discrimination task. We also report a novel canonical circuit in each mushroom body compartment with previously unidentified connections: reciprocal Kenyon cell to modulatory neuron connections, modulatory neuron to output neuron connections, and a surprisingly high number of recurrent connections between Kenyon cells. Stereotyped connections between output neurons could enhance the selection of learned responses. The complete circuit map of the mushroom body should guide future functional studies of this learning and memory center.Massively parallel, higher-order neuronal circuits such as the cerebellum and insect mushroom body serve to form and retain associations between stimuli and reinforcement in vertebrates and higher invertebrates [1][2][3][4][5][6] . Although these systems provide a biological substrate for adaptive behavior, no complete synapseresolution wiring diagram of their connectivity has been available to guide analysis and inspire understanding. The mushroom body (MB) is a higher-order parallel fiber system in many invertebrate brains, including hemimetabolous as well as holometabolous insects and their larval stages 6 . MB function is essential for associative learning in adult insects 1;3-5 and in Drosophila larvae 1;7;8 , from the earliest larval stages onward 9 . Indeed, the basic organization of the adult and the larval MB and their afferent circuits is very similar; however, larvae have about an order of magnitude fewer neurons 7 . Thus, to systematically investigate the organizational logic of the MB, we used serial section electron microscopy (EM) to map with synaptic resolution the complete MB connectome in a first instar Drosophila larva (L1; Fig. 1a). L1 are foraging animals capable of all behaviors previously described in later larval stages 10 , including adaptive behaviors dependent on associative learning 7;9 (Fig. 1b). Their smaller neurons enable fast EM imaging of the entire nervous system and reconstruction of complete circuits 11;12 . Models of sensory processing in many neural circuits feature neurons that fire in response to combinations of sensory inputs, generating a high-dimensional representation of the sensory environment 13 . The intrinsic MB neurons, the Kenyon cells (KCs), integrate in their dendrites inputs from combinations of projection neurons (PNs) that encode various stimuli, predominantly olfactory in both adult 1;4-6 , and larva 12;14 , but also thermal, gustatory
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