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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.
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This content will become publicly available on December 1, 2026
Drosophila DNp03 descending neurons serve as a hub within a flight saccade network
Animals rely on rapid sensorimotor processing to detect and respond to visual stimuli in their environment, yet how sensorimotor networks are organized to generate appropriate behaviors remains unclear. Here, we identify a bilateral pair of descending neurons (DNs), DNp03, as a hub for collision avoidance in flying flies. DNp03 receives visual information related to looming objects approaching on a collision course and connects directly and indirectly to motor neurons of the wings and neck, enabling the coordinated banked turn and head stabilization maneuvers of a rapid saccade. Although DNp03 can drive saccade-like behavior when optogenetically activated, naturalistic looming-evoked saccade behavior relies on a network of interconnected DNs that can partially compensate for DNp03 in its absence. The connectivity of this hierarchical network suggests DNp03 operates in parallel with two additional DN hubs that directly recruit subservient DNs to reinforce and expand behavioral outputs. We also find competition between the saccade network and descending pathways for landing behavior, where direct inhibitory connections from DNp03 reduce the likelihood a fly decides to land on, rather than turn away from, a looming object. Altogether, we provide a detailed mapping of one key sensorimotor pathway from visual inputs to motor outputs to demonstrate how even rapid, innate sensorimotor transformations rely on complex networks. These findings reveal intricate interconnectivity and hierarchy in descending pathways, a strategy that may represent a general principle of motor control across species.
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- Award ID(s):
- 1921065
- PAR ID:
- 10655857
- Publisher / Repository:
- Cell Press
- Date Published:
- Journal Name:
- Current Biology
- ISSN:
- 0960-9822
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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