Biology subjects

Dickinson, M. H.

Publications and source records attributed to Dickinson, M. H..

16 recordsLinked to original sources

bioRxiv2026

Flies evolved a gyrocompass to maintain navigational accuracy during rapid flight maneuvers

Halteres, the miniaturized hindwings of flies, function as biological gyroscopes that encode angular velocity during flight. Although their established role is to detect flight perturbations and trigger compensatory manoeuvers, here we show that halteres also function as a gyrocompass, maintaining an accurate estimate of heading during rapid turns. To overcome the incompatibility between rapid body rotations and two-photon imaging, we exploited the physics of haltere mechano-transduction to reproduce the inertial forces acting on the halteres during rapid body rotations using micron-scale oscillations of the thorax. Our experiments demonstrate that flies update their internal compass during rapid turns by integrating inertial measurements with predictions derived from efference copy signals. Because body saccades exceed the temporal bandwidth of visual motion processing, this inertial computation allows flies to maintain an accurate internal compass throughout these rapid manoeuvres. This capability may enable flies to compute critical parameters such as wind direction and ground speed by comparing measurements made before and after each saccade. Our findings suggest that an ancestral flight-stabilization system was evolutionarily co-opted into a biological gyrocompass, a new function that may have contributed to the adaptive radiation of flies.

neuroscience↗

bioRxiv2025

How tp1, an indirect wing steering muscle, stabilizes Drosophila's flight

Flapping flight is inherently unstable, requiring Drosophila to fine-tune their wing motions on a milliseconds timescale. Pioneering studies have shown that the direct steering muscles, which attach to the wing hinge, are important for generating these rapid flight reflexes. Recent connectome data, however, reveal that indirect steering muscles or tension muscles, which alter the mechanics of the thorax, receive some of the same synaptic inputs from the sensory apparatus as the direct steering muscles. This discovery suggests that the indirect steering muscles may also be important for flight control. Here, we show that the indirect tergopleural muscles indeed contribute substantially to stabilization, particularly for large pitch perturbations. We find that for small perturbations (less than 1000 deg/s), flies modulate their wing stroke amplitude to generate lift-based corrective torques, a strategy that has been previously documented. For larger perturbations, however, we observe that Drosophila engage an additional wing degree of freedom--the wing pitch angle--to leverage additional lift and drag forces during the corrective maneuver. Quasi-steady aerodynamic simulations reveal that this strategy minimizes power consumption, anaolgous to how some mammals (including humans) adjust their steady-state gaits in a near energy-optimal manner. Using optogenetics and a control theory framework we demonstrate that the tergopleural muscle is activated by a proportional gain component of a nonlinear PI controller responsible for determining the wing pitch angle during large perturbations. A simplified torsional-spring model for the wing hinge captures the changes in the wing pitch dynamics observed during correction maneuvers by using the tergopleural muscle to adjust the rest angle of the wing. These findings provide a striking example of reflex strategy selection in time-critical behaviors and underscores the vital role of indirect steering muscles in flight stabilization.

neuroscience↗

bioRxiv2023

Descending control and regulation of spontaneous flight turns in Drosophila

The clumped distribution of resources in the world has influenced the pattern of foraging behavior since the origins of life, selecting for a common locomotor search motif in which straight movements through resource-poor regions alternate with zig-zag exploration in resource-rich domains (Berg, 2000). For example, flies execute rapid changes in flight heading called body saccades during local search (Censi et al., 2013; Collett and Land, 1975; Schilstra and van Hateren, 1999; Wagner and Land, 1986), but suppress these turns during long-distance dispersal (Giraldo et al., 2018; Leitch et al., 2021) or when surging upwind after encountering an attractive odor plume (Budick and Dickinson, 2006; van Breugel and Dickinson, 2014). Here, we describe the key cellular components of a neural network in flies that generates spontaneous turns as well as a specialized neuron that inhibits the network to promote straight flight. Using 2-photon imaging, optogenetic activation, and genetic ablation, we show that only four descending neurons appear sufficient to generate the descending commands to execute flight saccades. The network is organized into two functional couplets--one for right turns and one for left--with each couplet consisting of an excitatory (DNae014) and inhibitory (DNb01) neuron that project to the flight motor neuropil within the ventral nerve cord. Using resources from recently published connectomes of the fly brain (Scheffer et al., 2020; Dorkenwald et al., 2023; Schlegel et al., 2023), we identified a large, unique interneuron (VES041) that forms inhibitory connections to all four saccade command neurons and created specific genetic driver lines for this cell. As predicted by its connectivity, activation of VES041 strongly suppresses saccades, suggesting that it regulates the transition between local search and long-distance dispersal. These results thus identify the critical elements of a network that not only structures the locomotor behavior of flies, but may also play a crucial role in their foraging ecology.

neuroscience↗

bioRxiv2023

Machine learning reveals the control mechanics of the insect wing hinge

Insects constitute the most species-rich radiation of metazoa, a success due to the evolution of active flight. Unlike pterosaurs, birds, and bats, the wings of insects did not evolve from legs1, but are novel structures attached to the body via a biomechanically complex hinge that transforms tiny, high-frequency oscillations of specialized power muscles into the sweeping back-and-forth motion of the wings2. The hinge consists of a system of tiny, hardened structures called sclerites that are interconnected to one another via flexible joints and regulated by the activity of specialized control muscles. Here, we imaged the activity of these muscles in a fly using a genetically encoded calcium indicator, while simultaneously tracking the 3D motion of the wings with high-speed cameras. Using machine learning approaches, we created a convolutional neural network3 that accurately predicts wing motion from the activity of the steering muscles, and an encoder-decoder4 that predicts the role of the individual sclerites on wing motion. By replaying patterns of wing motion on a dynamically scaled robotic fly, we quantified the effects of steering muscle activity on aerodynamic forces. A physics-based simulation that incorporates our model of the hinge generates flight maneuvers that are remarkably similar to those of free flying flies. This integrative, multi-disciplinary approach reveals the mechanical control logic of the insect wing hinge, arguably among the most sophisticated and evolutionarily important skeletal structures in the natural world.

neuroscience↗

bioRxiv2023

Single-cell type analysis of wing premotor circuits in the ventral nerve cord of Drosophila melanogaster

To perform most behaviors, animals must send commands from higher-order processing centers in the brain to premotor circuits that reside in ganglia distinct from the brain, such as the mammalian spinal cord or insect ventral nerve cord. How these circuits are functionally organized to generate the great diversity of animal behavior remains unclear. An important first step in unraveling the organization of premotor circuits is to identify their constituent cell types and create tools to monitor and manipulate these with high specificity to assess their functions. This is possible in the tractable ventral nerve cord of the fly. To generate such a toolkit, we used a combinatorial genetic technique (split-GAL4) to create 195 sparse transgenic driver lines targeting 196 individual cell types in the ventral nerve cord. These included wing and haltere motoneurons, modulatory neurons, and interneurons. Using a combination of behavioral, developmental, and anatomical analyses, we systematically characterized the cell types targeted in our collection. In addition, we identified correspondences between the cells in this collection and a recent connectomic data set of the ventral nerve cord. Taken together, the resources and results presented here form a powerful toolkit for future investigations of neuronal circuits and connectivity of premotor circuits while linking them to behavioral outputs.

neuroscience↗

bioRxiv2023

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.

neuroscience↗

bioRxiv2022

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.

neuroscience↗

bioRxiv2022

The role of a population of descending neurons in the optomotor response in flying Drosophila

To maintain stable flight, animals continuously perform trimming adjustments to compensate for internal and external perturbations. Whereas animals use many different sensory modalities to detect such perturbations, insects rely extensively on optic flow to modify their motor output and remain on course. We studied this behavior in the fruit fly, Drosophila melanogaster, by exploiting the optomotor response, a robust reflex in which an animal steers so as to minimize the magnitude of rotatory optic flow it perceives. Whereas the behavioral and algorithmic structure of the optomotor response has been studied in great detail, its neural implementation is not well-understood. In this paper, we present findings implicating a group of nearly homomorphic descending neurons, the DNg02s, as a core component for the optomotor response in flying Drosophila. Prior work on these cells suggested that they regulate the mechanical power to the flight system, presumably via connections to asynchronous flight motor neurons in the ventral nerve cord. When we chronically inactivated these cells, we observed that the magnitude of the optomotor response was diminished in proportion to the number of cells silenced, suggesting that the cells also regulate bilaterally asymmetric steering responses via population coding. During an optomotor response, flies coordinate changes in wing motion with movements of their head, abdomen, and hind legs, which are also diminished when the DNg02 cells are silenced. Using two-photon functional imaging, we show that the DNg02 cells respond most strongly to patterns of horizontal motion and that neuronal activity is closely correlated to motor output. However, unilateral optogenetic activation of DNg02 neurons does not elicit the asymmetric changes in wing motion characteristic of the optomotor response to a visual stimulus, but rather generates bilaterally symmetric increases in wingbeat amplitude. We interpret our experiments to suggest that flight maneuvers in flies require a more nuanced coordination of power muscles and steering muscles than previously appreciated, and that the physical flight apparatus of a fly might permit mechanical power to be distributed differentially between the two wings. Thus, whereas our experiments identify the DNg02 cells as a critical component of the optomotor reflex, our results suggest that other classes of descending cells targeting the steering muscle motor neurons are also required for the behavior.

neuroscience↗

bioRxiv2022

Neuromuscular embodiment of feedback control elements in Drosophila flight

While insects like Drosophila are flying, aerodynamic instabilities require that they make millisecond-timescale adjustments to their wing motion to stay aloft and on course. These stabilization reflexes can be modeled as a proportional-integral (PI) controller; however, it is unclear how such control might be instantiated in insects at the level of muscles and neurons. Here, we show that the b1 and b2 motor units--prominent components of the flys steering muscles system--modulate specific elements of the PI controller: the angular displacement (integral, I) and angular velocity (proportional, P), respectively. Moreover, these effects are observed only during the stabilization of pitch. Our results provide evidence for an organizational principle in which each muscle contributes to a specific functional role in flight control, a finding that highlights the power of using top-down behavioral modeling to guide bottom-up cellular manipulation studies.

animal behavior and cognition↗

bioRxiv2021

A population of descending neurons that regulate the flight motor of Drosophila

Like many insect species, Drosophila melanogaster are capable of maintaining a stable flight trajectory for periods lasting up to several hours(1, 2). Because aerodynamic torque is roughly proportional to the fifth power of wing length(3), even small asymmetries in wing size require the maintenance of subtle bilateral differences in flapping motion to maintain a stable path. Flies can even fly straight after losing half of a wing, a feat they accomplish via very large, sustained kinematic changes to the both damaged and intact wings(4). Thus, the neural network responsible for stable flight must be capable of sustaining fine-scaled control over wing motion across a large dynamic range. In this paper, we describe an unusual type of descending neurons (DNg02) that project directly from visual output regions of the brain to the dorsal flight neuropil of the ventral nerve cord. Unlike most descending neurons, which exist as single bilateral pairs with unique morphology, there is a population of at least 15 DNg02 cell pairs with nearly identical shape. By optogenetically activating different numbers of DNg02 cells, we demonstrate that these neurons regulate wingbeat amplitude over a wide dynamic range via a population code. Using 2-photon functional imaging, we show that DNg02 cells are responsive to visual motion during flight in a manner that would make them well suited to continuously regulate bilateral changes in wing kinematics. Collectively, we have identified a critical set of DNs that provide the sensitivity and dynamic range required for flight control.

neuroscience↗

bioRxiv2021

Drosophila local search emerges from iterative odometry of consecutive run lengths.

The ability to keep track of ones location in space is a critical behavior for animals navigating to and from a salient location, and its computational basis is now beginning to be unraveled. Here, we tracked flies in a ring-shaped channel as they executed bouts of search triggered by optogenetic activation of sugar receptors. Unlike experiments in open field arenas, which produce highly tortuous search trajectories, our geometrically constrained paradigm enabled us to monitor flies decisions to move toward or away from the fictive food. Our results suggest that flies use path integration to remember the location of a food site even after it has disappeared, and that flies can remember the location of a former food site even after walking around the arena one or more times. To determine the behavioral algorithms underlying Drosophila search, we developed multiple state transition models and found that flies likely accomplish path integration by combining odometry and compass navigation to keep track of their position relative to the fictive food. Our results indicate that whereas flies re-zero their path integrator at food when only one feeding site is present, they adjust their path integrator to a central location between sites when experiencing food at two or more locations. Together, this work provides a simple experimental paradigm and theoretical framework to advance investigations of the neural basis of path integration.

neuroscience↗

bioRxiv2020

The long-distance flight behavior of Drosophila suggests a general model for wind-assisted dispersal in insects.

Despite the ecological importance of long-distance dispersal in insects, its underlying mechanistic basis is poorly understood. One critical question is how insects interact with the wind to increase their travel distance as they disperse. To gain insight into dispersal using a species amenable to further investigation using genetic tools, we conducted release-and-recapture experiments in the Mojave Desert using the fruit fly, Drosophila melanogaster. We deployed chemically-baited traps in a 1 km-radius ring around the release site, equipped with machine vision systems that captured the arrival times of flies as they landed. In each experiment, we released between 30,000 and 200,000 flies. By repeating the experiments under a variety of conditions, we were able to quantify the influence of wind on flies’ dispersal behavior. Our results confirm that even tiny fruit flies could disperse ∼15 km in a single flight in still air, and might travel many times that distance in a moderate wind. The dispersal behavior of the flies is well explained by a model in which animals maintain a fixed body orientation relative to celestial cues, actively regulate groundspeed along their body axis, and allow the wind to advect them sideways. The model accounts for the observation that flies actively fan out in all directions in still air, but are increasingly advected downwind as winds intensify. In contrast, our field data do not support a Lévy flight model of dispersal, despite the fact that our experimental conditions almost perfectly match the core assumptions of that theory.Significance Statement Flying insects play a vital role in terrestrial ecosystems, and their decline over the past few decades has been implicated in a collapse of many species that depend upon them for food. By dispersing over large distances, insects transport biomass from one region to another and thus their flight behavior influences ecology on a global scale. Our experiments provide key insight into the dispersal behavior of insects, and suggest that these animals employ a single algorithm that is functionally robust in both still air and under windy conditions. Our results will make it easier to study the ecologically important phenomenon of long-distance dispersal in a genetic model organism, facilitating the identification of cellular and genetic mechanisms.Competing Interest StatementThe authors have declared no competing interest.View Full Text

animal behavior and cognition↗

bioRxiv2018

Diverse food-sensing neurons trigger idiothetic local search in Drosophila

Resources are often sparsely clustered in nature. Thus, foraging animals may benefit from remembering the location of a newly discovered food patch while continuing to explore nearby [1, 2]. For example, after encountering a drop of yeast or sugar, hungry flies often perform a local search consisting of frequent departures and returns to the food site [3, 4]. Fruit flies, Drosophila melanogaster, can perform this food-centered search behavior in the absence of external stimuli or landmarks, instead relying solely on internal (idiothetic) cues to keep track of their location [5]. This path integration behavior may represent a deeply conserved navigational capacity in insects [6, 7], but the neural pathways underlying food-triggered searches remain unknown. Here, we used optogenetic activation to screen candidate cell classes and found that local searches can be initiated by diverse sensory neurons including sugar-sensors, water-sensors, olfactory-receptor neurons, as well as hunger-signaling neurons of the central nervous system. Optogenetically-induced searches resemble those triggered by actual food and are modulated by starvation state. Furthermore, search trajectories exhibit key features of path integration: searches remain tightly centered around the fictive-food site, even during long periods without reinforcement, and flies re-center their searches when they encounter a new fictive-food site. Flies can even perform elaborate local searches within a constrained maze. Together, these results suggest that flies enact local searches in response to a wide variety of food-associated cues, and that these sensory pathways may converge upon a common neural system for path integration. Optogenetically induced local searches in Drosophila can now serve as a tractable system for the study of spatial memory and navigation in insects.

animal behavior and cognition↗

bioRxiv2018

Imaging neural activity in the ventral nerve cord of behaving adult Drosophila

To understand neural circuits that control limbs, one must measure their activity during behavior. Until now this goal has been challenging, because the portion of the nervous system that contains limb premotor and motor circuits is largely inaccessible to large-scale recording techniques in intact, moving animals - a constraint that is true for both vertebrate and invertebrate models. Here, we introduce a method for 2-photon functional imaging from the ventral nerve cord of behaving adult Drosophila melanogaster. We use this method to reveal patterns of activity across nerve cord populations during grooming and walking and to uncover the functional encoding of moonwalker ascending neurons (MANs), moonwalker descending neurons (MDNs), and a novel class of locomotion-associated descending neurons. This new approach enables the direct investigation of circuits associated with complex limb movements.

neuroscience↗

bioRxiv2017

The functional organization of descending sensory-motor pathways in Drosophila

In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck and terminate in post-cranial regions of the nervous system. This critical neural population is thought to activate, maintain and modulate locomotion and other behaviors. Although individual members of this cell class have been well-studied across species ranging from insects to primates, little is known about the overall connectivity pattern of DNs as a population. We undertook a systematic anatomical investigation of descending neurons in the fruit fly, Drosophila melanogaster, and created a collection of over 100 transgenic lines targeting individual cell types. Our methods allowed us to describe the morphology of roughly half of an estimated 400 DNs and create a comprehensive map of connectivity between the sensory neuropils in the brain and the motor neuropils in the ventral nerve cord. Like the vertebrate spinal cord, our results show that the fly nerve cord is a highly organized, layered system of neuropils, an organization that reflects the fact that insects are capable of two largely independent means of locomotion - walking and fight - using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of sensory-motor circuits.

neuroscience↗

bioRxiv2017

Drosophila have distinct activity-gated pathways that mediate attraction and aversion to CO2

Carbon dioxide is a volatile and broad signal of many organic processes, and serves as a convenient cue for insects in search of blood hosts1-6, flowers7, decaying matter8-11, communal nests12, fruit13, and wildfires14. Curiously, although Drosophila melanogaster feed on yeast that produce CO2 and ethanol during fermentation, laboratory experiments suggest that flies actively avoid CO215-25. Here, we resolve this paradox by showing that both flying and walking fruit flies do actually find CO2 attractive, but only when they are in an active state associated with foraging. Aversion at low activity levels may be an adaptation to avoid CO2-seeking-parasites, or succumbing to respiratory acidosis in the presence of high concentrations of CO2 that are occasionally found in nature26,27. In contrast to CO2, flies are attracted to ethanol in all behavioral states, and invest twice as much time searching near ethanol compared to CO2. These behavioral differences reflect the fact that whereas CO2 is a generated by many natural processes, ethanol is a unique signature of yeast fermentation. Using genetic tools, we determined that the evolutionarily ancient ionotropic co-receptor IR25a is required for both CO2 and ethanol attraction, and that the receptors previously identified for CO2 avoidance are not involved. Our study lays the foundation for future research to determine the neural circuits underlying both state- and odorant-dependent decision making in Drosophila.

neuroscience↗