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Insects exhibit remarkable sensory , motor capabilities to successfully navigate their environment. As insects move, they activate sensory afferents. Hence, insects are inextricably part of their sensory ecology. Insects must correctly attribute self -versus external sources of sensory activation to make adaptive behavioral choices. This is achieved via corollary discharge circuits (CDCs), motor-to-sensory neuronal pathways providing predictive motor signals to sensory networks to coordinate sensory processing within the context of ongoing behavior. While CDCs provide predictive motor signals, their underlying mechanisms of action and functional consequences are diverse. Here, we describe inferred CDCs and identified corollary discharge interneurons (CDIs) in insects, highlighting their anatomical commonalities and our limited understanding of their synaptic integration into the nervous system. By using connectomics information, we demonstrate that the complexity with which identified CDIs integrate into the central nervous system (CNS) can be revealed. 

Natural behaviors are a coordinated symphony of motor acts that drive reafferent (self-induced) sensory activation. Individual sensors cannot disambiguate exafferent (externally induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to carry out adaptive behaviors through corollary discharge circuits (CDCs), which provide predictive motor signals from motor pathways to sensory processing and other motor pathways. Yet, how CDCs comprehensively integrate into the nervous system remains unexplored. Here, we use connectomics, neuroanatomical, physiological, and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs) in Drosophila, which function as a predictive CDC in other insects. Both AHN pairs receive input primarily from a partially overlapping population of descending neurons, especially from DNg02, which controls wing motor output. Using Ca2+ imaging and behavioral recordings, we show that AHN activation is correlated to flight behavior and precedes wing motion. Optogenetic activation of DNg02 is sufficient to activate AHNs, indicating that AHNs are activated by descending commands in advance of behavior and not as a consequence of sensory input. Downstream, each AHN pair targets predominantly non-overlapping networks, including those that process visual, auditory, and mechanosensory information, as well as networks controlling wing, haltere, and leg sensorimotor control. These results support the conclusion that the AHNs provide a predictive motor signal about wing motor state to mostly non-overlapping sensory and motor networks. Future work will determine how AHN signaling is driven by other descending neurons and interpreted by AHN downstream targets to maintain adaptive sensorimotor performance.