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Dallmann, C. J.

Publications and source records attributed to Dallmann, C. J..

7 recordsLinked to original sources

A dedicated brain circuit controls forward walking in Drosophila

Neural circuits in the brain control high-level parameters of movement, including the initiation, speed, and direction of locomotion. How specific cell types are organized into circuits to compute these control signals and enable context-appropriate behavior remains unclear. Here, we identify central brain neurons in Drosophila that can initiate walking and exert graded control over walking speed. Connectome analyses position the neurons on top of a layered brain circuit, which recruits a specific population of descending neurons to control forward walking independently of turning and other parameters. As predicted by the connectome, the circuit enforces straight walking when activated unilaterally, and the activity of the central brain neurons represents a high-level walking drive. This drive is suppressed during flight but flexibly integrated with other control signals to enable complex movement sequences during obstacle negotiation. Together, our findings elucidate a dedicated brain circuit that enables efficient computation, selection, and integration of forward-walking signals for context-appropriate motor control.

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Parallel neuronal ensembles control behavior across sensorimotor levels in Drosophila

Nervous systems can process information in serial or in parallel, trading off efficiency for flexibility and speed. How these network architectures are implemented across sensorimotor pathways to control behavior is unclear. We investigate this tradeoff directly in Drosophila by comparing neuronal circuits underlying landing and takeoff, behaviors transforming similar visual cues to whole-body motor output. Using a whole-CNS connectome, electrophysiology, and behavioral analysis, we reconstruct the complete feedforward pathway for landing, including visual feature detectors, a dedicated ensemble of descending neurons (DNs), and a core premotor circuit in the nerve cord. Comparison to the takeoff pathway reveals that, despite encoding the same sensory feature and engaging similar muscle groups, neuronal circuits controlling the two behaviors are separated at every sensorimotor level. Extending this analysis to the complete DN population reveals a blueprint for descending motor control: DNs across the behavioral space utilized by the fly are organized as a set of parallel, loosely-overlapping ensembles that form a continuum from command-like control, with individual DNs determining behavioral output, to population coding, with multiple DNs controlling behavior synergistically. Distinct combinations of sensory feature detectors differentially recruit DN ensembles to enable flexible, context-dependent behavioral control.

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Proprioceptive limit detectors mediate sensorimotor control of the Drosophila leg

Many animals possess mechanosensory neurons that fire when a limb nears the limit of its physical range, but the function of these proprioceptive limit detectors remains poorly understood. Here, we investigate a class of proprioceptors on the Drosophila leg called hair plates. Using calcium imaging in behaving flies, we find that a hair plate on the fly coxa (CxHP8) detects the limits of anterior leg movement. Reconstructing CxHP8 axons in the connectome, we found that they are wired to excite posterior leg movement and inhibit anterior leg movement. Consistent with this connectivity, optogenetic activation of CxHP8 neurons elicited posterior postural reflexes, while silencing altered the swing-to-stance transition during walking. Finally, we use comprehensive reconstruction of peripheral morphology and downstream connectivity to predict the function of other hair plates distributed across the fly leg. Our results suggest that each hair plate is specialized to control specific sensorimotor reflexes that are matched to the joint limit it detects. They also illustrate the feasibility of predicting sensorimotor reflexes from a connectome with identified proprioceptive inputs and motor outputs.

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Divergent neural circuits for proprioceptive and exteroceptive sensing of the Drosophila leg

Somatosensory neurons provide the nervous system with information about mechanical forces originating inside and outside the body. Here, we use connectomics from electron microscopy to reconstruct and analyze neural circuits downstream of the largest somatosensory organ in the Drosophila leg, the femoral chordotonal organ (FeCO). The FeCO has been proposed to support both proprioceptive sensing of the flys femur-tibia joint and exteroceptive sensing of substrate vibrations, but it was unknown which sensory neurons and central circuits contribute to each of these functions. We found that different subtypes of FeCO sensory neurons feed into distinct proprioceptive and exteroceptive pathways. Position- and movement-encoding FeCO neurons connect to local leg motor control circuits in the ventral nerve cord (VNC), indicating a proprioceptive function. In contrast, signals from the vibration-encoding FeCO neurons are integrated across legs and transmitted to mechanosensory regions in the brain, indicating an exteroceptive function. Overall, our analyses reveal the structure of specialized circuits for processing proprioceptive and exteroceptive signals from the fly leg. These findings are consistent with a growing body of work in invertebrate and vertebrate species demonstrating the existence of specialized limb mechanosensory pathways for sensing external vibrations.

neuroscience↗

Presynaptic inhibition selectively suppresses leg proprioception in behaving Drosophila

Controlling arms and legs requires feedback from proprioceptive sensory neurons that detect joint position and movement. Proprioceptive feedback must be tuned for different behavioral contexts, but the underlying circuit mechanisms remain poorly understood. Using calcium imaging in behaving Drosophila, we find that the axons of position-encoding leg proprioceptors are active across behaviors, whereas the axons of movement-encoding leg proprioceptors are suppressed during walking and grooming. Using connectomics, we identify a specific class of interneurons that provide GABAergic presynaptic inhibition to the axons of movement-encoding proprioceptors. The predominant synaptic inputs to these interneurons are descending neurons, suggesting they are driven by predictions of leg movement originating in the brain. Calcium imaging from both the interneurons and their descending inputs confirmed that their activity is correlated with self-generated but not passive leg movements. Overall, our findings elucidate a neural circuit for suppressing specific proprioceptive feedback signals during self-generated movements.

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Synaptic architecture of leg and wing motor control networks in Drosophila

Animal movement is controlled by motor neurons (MNs), which project out of the central nervous system to activate muscles. MN activity is coordinated by complex premotor networks that allow individual muscles to contribute to many different behaviors. Here, we use connectomics to analyze the wiring logic of premotor circuits controlling the Drosophila leg and wing. We find that both premotor networks cluster into modules that link MNs innervating muscles with related functions. Within most leg motor modules, the synaptic weights of each premotor neuron are proportional to the size of their target MNs, establishing a circuit basis for hierarchical MN recruitment. In contrast, wing premotor networks lack proportional synaptic connectivity, which may allow wing steering muscles to be recruited with different relative timing. By comparing the architecture of distinct limb motor control systems within the same animal, we identify common principles of premotor network organization and specializations that reflect the unique biomechanical constraints and evolutionary origins of leg and wing motor control.

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Tools for comprehensive reconstruction and analysis of Drosophila motor circuits

Like the vertebrate spinal cord, the insect ventral nerve cord (VNC) mediates limb sensation and motor control. Here, we apply automated tools for electron microscopy volume alignment, neuron segmentation, and synapse prediction toward creating a connectome of an adult female Drosophila VNC. To interpret a connectome, it is crucial to know its relationship with the rest of the body. We therefore mapped the muscle targets of leg and wing motor neurons in the connectome by comparing their morphology to genetic driver lines, dye fills, and X-ray nano-tomography of the fly leg and wing. Knowing the outputs of the connectome allowed us to identify neural circuits that coordinate the wings and legs during escape takeoff. We provide the reconstruction of VNC circuits and motor neuron atlas, along with tools for programmatic and interactive access, as community resources to support experimental and theoretical studies of how the fly nervous system controls behavior.

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