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Suver, M. P.

Publications and source records attributed to Suver, M. P..

5 recordsLinked to original sources

Motor control of the Drosophila antennae

Animals actively sense their surroundings to acquire behaviorally relevant environmental cues and stimuli. This dynamic acquisition of sensory information is enabled by active positioning of sensors and helps guide behavioral responses in dynamic environments. Yet how these active movements are controlled during behavior and coordinated with ongoing sensory acquisition is not fully understood. In the fruit fly Drosophila melanogaster, the antennae are crucial sensors for extracting important information from the environment including mechanosensory, olfactory, and auditory signals. Just four distinct muscles command movement of the antennae, providing a tractable model system for understanding efferent control of sensation. This work characterizes motor neurons used by Drosophila to actively position the antennae. We first identify antennal motor neurons in the central brain, and map each one from a comprehensive connectomic dataset to its peripheral muscle target. Our analysis of presynaptic inputs to the entire antennal motor system reveals a diverse array of premotor neurons for antennal motor control. We then provide genetic access to each motor unit by building a library of genetic lines with expression in antennal motor neurons. Using this library of antennal motor neuron lines, we next characterize motor unit function with quantitative behavior and optogenetics, revealing that the antennal motor system produces two primary movements in the dorsal-ventral and medial-lateral axes. Together, this work provides a comprehensive framework for understanding the motor control of an active sensor.

neuroscience↗

Sensory-motor integration in a nonspiking interneuron contributes to active sensor control in Drosophila

An animals nervous system enables it to detect and respond to stimuli to navigate its environment. To enhance sensory acquisition, animals can actively position sensors, altering how they extract information from the external world. However, active sensing, and movement in general, produces sensory feedback, requiring mechanisms for integrating predictive motor signals with externally generated sensations. Despite the importance of these mechanisms for guiding coordinated behavior, the cellular and circuit basis of motor control and sensory processing during active movements are not fully understood. Here, we investigate how mechanosensory information contributes to motor output in the Drosophila antenna, a sensor that can be actively positioned. We combine electrophysiology, quantitative behavior, optogenetics, and connectomics to characterize APN2, a nonspiking interneuron in Drosophila that encodes both mechanosensory stimuli and motor commands. We show that these neurons receive input from two classes of antennal mechanosensors, enabling responses to mechanical perturbations in both quiescence and flight. We then demonstrate how these neurons integrate higher-order motor commands with mechanosensory input to shape antennal movement. Together, this work reveals a previously uncharacterized sensory-motor circuit in the antennal mechanosensory system. These findings provide insight into how nervous systems integrate sensation with motor commands to guide the movement of active sensors, highlighting circuit mechanisms that may broadly support sensory acquisition during movement.

neuroscience↗

Multisensory integration for active mechanosensation in Drosophila flight

To support robust behaviors in highly variable environments, animals rely on active sampling of their sensory surroundings. Here, we use tethered, flying Drosophila melanogaster and a multisensory behavioral apparatus simulating forward flight to determine how visual and mechanosensory information are integrated and control active movements of an important multimodal sensory organ, the antennae. We found that flies perform active antennal movements in response to varying airflow, and that the direction of these movements changes depending on the visual environment. Next, we found that antennal movements are amplified in the presence of visual motion, but only when the fly was flying. Through mechanical and optogenetic manipulation of mechanosensory input, we found that mechanosensory feedback is vital to antennal positioning at flight onset. Additionally, we observed unexpected changes in wingbeat frequency when the antenna was mechanically stabilized, suggesting that multiple antennal mechanosensors contribute to flight regulation. Finally, we show that integration of mechanosensory and visual cues for controlling antennal motion follows in a "winner-takes-all" paradigm dependent on the stimulus frequency, mirroring visuo-mechanosensory guided behaviors in other species. Together, these results reveal novel behavioral gating of sensory information and expand our understanding of the efferent control of active sensing.

neuroscience↗

Active antennal movements in Drosophila tune wind encoding

Many insects actively move their antennae, but how these movements influence sensory encoding is not fully understood. Antennae are used to smell odors1,2, detect auditory cues3,4, and sense mechanosensory stimuli such as wind5 and objects6-8, frequently by combining active movement with sensation. Genetic access to antennal motor systems would thus provide a powerful tool for dissecting the circuit mechanisms underlying active sensing, but little is known about how the most genetically tractable insect, Drosophila melanogaster, moves its antennae. Here we use DeepLabCut to measure how tethered Drosophila move their antennae in the presence of sensory stimuli, and identify genetic reagents for controlling antennal movement. We find that flies perform both slow and fast antennal movements in response to wind-induced deflections, but not the attractive odor apple cider vinegar. We describe four muscles in the first antennal segment that control antennal movements, and identify genetic driver lines that provide access to two groups of antennal motor neurons and an antennal muscle. Through optogenetic inactivation, we provide evidence that antennal motor neurons are specialized for different movement speeds. Finally, we show that activation of antennal motor neurons and muscles can improve the gain and acuity of wind direction encoding. Together, our experiments provide insight into the neural control of antennal movement and suggest that Drosophila actively position their antennae to tune the precision of wind encoding.

neuroscience↗

Encoding of wind direction by central neurons in Drosophila

Wind is a major navigational cue for insects, but how wind direction is decoded by central neurons in the insect brain is unknown. Here, we find that walking flies combine signals from both antennae to orient to wind during olfactory search behavior. Movements of single antennae are ambiguous with respect to wind direction, but the difference between left and right antennal displacements yields a linear code for wind direction in azimuth. Second-order mechanosensory neurons share the ambiguous responses of single antenna and receive input primarily from the ipsilateral antenna. Finally, we identify a novel set of neurons, which we call wedge projection neurons, that integrate signals across the two antennae and receive input from at least three classes of second-order neurons to produce a more linear representation of wind direction. This study establishes how a feature of the sensory environment - the wind direction - is decoded by single neurons that compare information across two sensors.

neuroscience↗