Flight Motor Research Articles

The Hawkmoth Proboscis: An Insect Model for Sensorimotor Control of Reaching and Exploration.

Reaching and inspecting objects is an intricate part of human life, which is shared by a diversity of animals across phyla. In addition to appendages like legs and antennae, some insects use their mouthparts to reach and inspect targets. Hawkmoths of the family Sphingidae (Lepidoptera) use their extremely long and straw-like proboscis to drink nectar from flowers. As they approach flowers, hawkmoths uncoil their proboscis and explore the floral surface while hovering to target the proboscis to the nectary hole. Several sensory modalities provide feedback to control and guide these extremely versatile proboscis movements. The control task faced by the hawkmoths' nervous system during such behaviors is not unlike that of an animal guiding limbs or a robotic agent guiding a manipulator to a target. Hawkmoths perform these reaching maneuvers while simultaneously hovering, and hence require rapid and continuous coordination between the proboscis, neck, and flight motor systems, thereby providing a unique invertebrate model for studying appendage guidance and reaching. Here, we review what is known about how hawkmoths use their proboscis for floral inspection and nectar discovery, as well as the role of various sensors in proboscis guidance. We give a brief overview of the morphology and muscular apparatus of the hawkmoth proboscis, and discuss how multimodal sensory feedback might be turned into motor action for appendage guidance.

Organization of an ascending circuit that conveys flight motor state in Drosophila

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.

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 locomotion, selecting for a common search motif in which straight movements through resource-poor regions alternate with zig-zag exploration in resource-rich domains. For example, during local search, flying flies spontaneously execute rapid flight turns, called body saccades, but suppress these maneuvers during long-distance dispersal or when surging upstream toward an attractive odor. Here, we describe the key cellular components of a neural network in flies that generate spontaneous turns as well as a specialized pair of neurons that inhibits the network and suppresses turning. 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 units-one for right turns and one for left-with each unit consisting of an excitatory (DNae014) and an inhibitory (DNb01) neuron that project to the flight motor neuropil within the ventral nerve cord. Using resources from recently published connectomes of the fly, we identified a pair of large, distinct interneurons (VES041) that form 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 promotes straight flight to regulate the transition between local search and long-distance dispersal. These results thus identify the key elements of a network that may play a crucial role in foraging ecology.

The self-oscillation paradox in the flight motor of Drosophila melanogaster.

Tiny flying insects, such as Drosophila melanogaster, fly by flapping their wings at frequencies faster than their brains are able to process. To do so, they rely on self-oscillation: dynamic instability, leading to emergent oscillation, arising from muscle stretch-activation. Many questions concerning this vital natural instability remain open. Does flight motor self-oscillation necessarily lead to resonance-a state optimal in efficiency and/or performance? If so, what state? And is self-oscillation even guaranteed in a motor driven by stretch-activated muscle, or are there limiting conditions? In this work, we use data-driven models of wingbeat and muscle behaviour to answer these questions. Developing and leveraging novel analysis techniques, including symbolic computation, we establish a fundamental condition for motor self-oscillation common to a wide range of motor models. Remarkably, D. melanogaster flight apparently defies this condition: a paradox of motor operation. We explore potential resolutions to this paradox, and, within its confines, establish that the D. melanogaster flight motor is probably not resonant with respect to exoskeletal elasticity: instead, the muscular elasticity plays a dominant role. Contrary to common supposition, the stiffness of stretch-activated muscle is an obstacle to, rather than an enabler of, the operation of the D. melanogaster flight motor.

Compensation for a costly ornament depends on the development of flight performance in stalk-eyed flies

Several species of stalk-eyed flies exhibit exaggerated sexual dimorphism where females favor males with longer eyespans. Longer eyespan increases a fly’s moment of inertia, and may, therefore, impact flight behavior and fitness, specifically maneuverability and predator evasion. However, these putative costs may be ameliorated by co-selection for compensatory traits, as flies with longer eyespans tend to have larger thoraces and wings, which allows them to perform turns similar to flies with shorter eyespans. Furthermore, the capacity to compensate for a potentially costly ornament may not be fixed across the life-history of the adult stage, as stalk-eyed flies achieve sexual maturity at 3-4 weeks of age, accompanied by significant growth of reproductive tissues and organs. Thus, growth of the abdomen and body mass over time may impose constraints on flight performance that may affect whether an adult reaches the age of reproductive viability. The purpose of this study was to investigate the flight performance of stalk-eyed flies and its relationship to body morphology and development. The flight performance of 1-to-30 day oldTeleopsis dalmanni(n=124) andDiasemopsis meigenii(n=83) were assessed by presenting normoxic, variable-density mixtures of heliox (O2, N2and He) in 10% increments ranging from air to pure heliox; the least-dense gas allowing flight represented maximal performance. Flight kinematics were analyzed using high-speed (5930fps) videography. Immediately following flight assessment, flies were euthanized, photographed, dissected and weighed. In both species, total body mass, thorax and abdominal mass increased across age. Wing kinematics and maximal flight capacity were associated with thorax mass, and increased with age as flies became heavier. Although flies with longer eyespans were indeed heavier, they had larger wings and thoraces; however, maximal flight capacity and kinematics were generally independent of eyespan. Thus, bearing long eye-stalks did not impair flight performance, nor did the increase in mass attributable to reproductive maturation. Instead, variation in flight performance appears associated with the development of the flight motor, and improved ratio of thorax-to-total mass, across age.

Solving the thoracic inverse problem in the fruit fly

In many insect species, the thoracic exoskeletal structure plays a crucial role in enabling flight. In the dipteran indirect flight mechanism, thoracic cuticle acts as a transmission link between the flight muscles and the wings, and is thought to act as an elastic modulator: improving flight motor efficiency thorough linear or nonlinear resonance. But peering closely into the drivetrain of tiny insects is experimentally difficult, and the nature of this elastic modulation is unclear. Here, we present a new inverse-problem methodology to surmount this difficulty. In a data synthesis process, we integrate literature-reported rigid-wing aerodynamic and musculoskeletal data into a planar oscillator model for the fruit fly Drosophila melanogaster, and use this integrated data to identify several surprising properties of the fly’s thorax. We find that fruit flies likely have an energetic need for motor resonance: absolute power savings due to motor elasticity range from 0%–30% across literature-reported datasets, averaging 16%. However, in all cases, the intrinsic high effective stiffness of the active asynchronous flight muscles accounts for all elastic energy storage required by the wingbeat. The D. melanogaster flight motor should be considered as a system in which the wings are resonant with the elastic effects of the motor’s asynchronous musculature, and not with the elastic effects of the thoracic exoskeleton. We discover also that D. melanogaster wingbeat kinematics show subtle adaptions that ensure that wingbeat load requirements match muscular forcing. Together, these newly-identified properties suggest a novel conceptual model of the fruit fly’s flight motor: a structure that is resonant due to muscular elasticity, and is thereby intensely concerned with ensuring that the primary flight muscles are operating efficiently. Our inverse-problem methodology sheds new light on the complex behaviour of these tiny flight motors, and provides avenues for further studies in a range of other insect species.

Distinct forms of resonant optimality within insect indirect flight motors.

Insect flight motors are extraordinary natural structures that operate efficiently at high frequencies. Structural resonance is thought to play a role in ensuring efficient motor operation, but the details of this role are elusive. While the efficiency benefits associated with resonance may be significant, a range of counterintuitive behaviours are observed. In particular, the relationship between insect wingbeat frequencies and thoracic natural frequencies is uncertain, with insects showing wingbeat frequency modulation over both short and long time scales. Here, we offer new explanations for this modulation. We show how, in linear and nonlinear models of an indirect flight motor, resonance is not a unitary state at a single frequency, but a complex cluster of distinct and mutually exclusive states, each representing a different form of resonant optimality. Additionally, by characterizing the relationship between resonance and the state of negative work absorption within the motor, we demonstrate how near-perfect resonant energetic optimality can be maintained over significant wingbeat frequency ranges. Our analysis leads to a new conceptual model of flight motor operation: one in which insects are not energetically restricted to a precise wingbeat frequency, but instead are robust to changes in thoracic and environmental properties-an illustration of the extraordinary robustness of these natural motors.

Insect flight: Flies use a throttle to steer

A new study of flight control in Drosophila using neurogenetic methods and a virtual reality flight arena has revealed a group of descending neurons that fully activate the flight motor and steer the fly by independent regulation of the left and right wings.

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

SummaryLike many insect species, Drosophila melanogaster are capable of maintaining a stable flight trajectory for periods lasting up to several hours1,2. Because aerodynamic torque is roughly proportional to the fifth power of wing length3, 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 both the damaged and intact wings4. 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 neuron (DNg02) that projects directly from visual output regions of the brain to the dorsal flight neuropil of the ventral nerve cord. Unlike many 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.

Flight motor demonstration for direct-injection gas-hybrid rocket

Flight motor demonstration for direct-injection gas-hybrid rocket

Precise timing is ubiquitous, consistent, and coordinated across a comprehensive, spike-resolved flight motor program

Sequences of action potentials, or spikes, carry information in the number of spikes and their timing. Spike timing codes are critical in many sensory systems, but there is now growing evidence that millisecond-scale changes in timing also carry information in motor brain regions, descending decision-making circuits, and individual motor units. Across all of the many signals that control a behavior, how ubiquitous, consistent, and coordinated are spike timing codes? Assessing these open questions ideally involves recording across the whole motor program with spike-level resolution. To do this, we took advantage of the relatively few motor units controlling the wings of a hawk moth, Manduca sexta. We simultaneously recorded nearly every action potential from all major wing muscles and the resulting forces in tethered flight. We found that timing encodes more information about turning behavior than spike count in every motor unit, even though there is sufficient variation in count alone. Flight muscles vary broadly in function as well as in the number and timing of spikes. Nonetheless, each muscle with multiple spikes consistently blends spike timing and count information in a 3:1 ratio. Coding strategies are consistent. Finally, we assess the coordination of muscles using pairwise redundancy measured through interaction information. Surprisingly, not only are all muscle pairs coordinated, but all coordination is accomplished almost exclusively through spike timing, not spike count. Spike timing codes are ubiquitous, consistent, and essential for coordination.

Motor output and control input in flapping flight: a compact model of the deforming wing kinematics of manoeuvring hoverflies.

Insects are conventionally modelled as controlling flight by varying a few summary kinematic parameters that are defined on a per-wingbeat basis, such as the stroke amplitude, mean stroke angle and mean wing pitch angle. Nevertheless, as insects have tens of flight muscles and vary their kinematics continuously, the true dimension of their control input space is likely to be much higher. Here, we present a compact description of the deforming wing kinematics of 36 manoeuvring Eristalis hoverflies, applying functional principal components analysis to Fourier series fits of the wingtip position and wing twist measured over 26 541 wingbeats. This analysis offers a high degree of data reduction, in addition to insight into the natural kinematic couplings. We used statistical resampling techniques to verify that the principal components (PCs) were repeatable features of the data, and analysed their coefficient vectors to provide insight into the form of these natural couplings. Conceptually, the dominant PCs provide a natural set of control input variables that span the control input subspace utilized by this species, but they can also be thought of as output states of the flight motor. This functional description of the wing kinematics is appropriate to modelling insect flight as a form of limit cycle control.

State-dependent decoupling of sensory and motor circuits underlies behavioral flexibility in Drosophila.

An approaching predator and self-motion towards an object can generate similar looming patterns on the retina, but these situations demand different rapid responses. How central circuits flexibly process visual cues to activate appropriate, fast motor pathways remains unclear. Here, we identify two descending neuron (DN) types that control landing and contribute to visuomotor flexibility in Drosophila. For each, silencing impairs visually-evoked landing, activation drives landing, and spike rate determines leg extension amplitude. Critically, visual responses of both DNs are severely attenuated during non-flight periods, effectively decoupling visual stimuli from the landing motor pathway when landing is inappropriate. The flight-dependence mechanism differs between DN types. Octopamine exposure mimics flight effects in one, whereas the other likely receives neuronal feedback from flight motor circuits. Thus, this sensorimotor flexibility arises from distinct mechanisms for gating action-specific descending pathways, such that sensory and motor networks are coupled or decoupled according to the behavioral state.

Distinctions among electroconvulsion- and proconvulsant-induced seizure discharges and native motor patterns during flight and grooming: quantitative spike pattern analysis in Drosophila flight muscles

In Drosophila, high-frequency electrical stimulation across the brain triggers a highly stereotypic repertoire of spasms. These electroconvulsive seizures (ECS) manifest as distinctive spiking discharges across the nervous system and can be stably assessed throughout the seizure repertoire in the large indirect flight muscles dorsal longitudinal muscles (DLMs) to characterize modifications in seizure-prone mutants. However, the relationships between ECS-spike patterns and native motor programs, including flight and grooming, are not known and their similarities and distinctions remain to be characterized. We employed quantitative spike pattern analyses for the three motor patterns including: (1) overall firing frequency, (2) spike timing between contralateral fibers, and (3) short-term variability in spike interval regularity (CV2) and instantaneous firing frequency (ISI−1). This base-line information from wild-type (WT) flies facilitated quantitative characterization of mutational effects of major neurotransmitter systems: excitatory cholinergic (Cha), inhibitory GABAergic (Rdl) and electrical (ShakB) synaptic transmission. The results provide an initial glimpse on the vulnerability of individual motor patterns to different perturbations. We found marked alterations of ECS discharge spike patterns in terms of either seizure threshold, spike frequency or spiking regularity. In contrast, no gross alterations during grooming and a small but noticeable reduction of firing frequency during Rdl mutant flight were found, suggesting a role for GABAergic modulation of flight motor programs. Picrotoxin (PTX), a known pro-convulsant that inhibits GABAA receptors, induced DLM spike patterns that displayed some features, e.g. left-right coordination and ISI−1 range, that could be found in flight or grooming, but distinct from ECS discharges. These quantitative techniques may be employed to reveal overlooked relationships among aberrant motor patterns as well as their links to native motor programs.

Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

Insect flight is a complex behavior that requires the integration of multiple sensory inputs with flight motor output. Although previous genetic studies identified central brain monoaminergic neurons that modulate Drosophila flight, neuro-modulatory circuits underlying sustained flight bouts remain unexplored. Certain classes of dopaminergic and octopaminergic neurons that project to the mushroom body, a higher integrating center in the insect brain, are known to modify neuronal output based on contextual cues and thereby organismal behavior. This study focuses on how monoaminergic modulation of mushroom body GABAergic output neurons (MBONs) regulates the duration of flight bouts. Octopaminergic neurons in the sub-esophageal zone stimulate central dopaminergic neurons (protocerebral anterior medial, PAM) that project to GABAergic MBONs. Either inhibition of octopaminergic and dopaminergic neurons or activation of GABAergic MBONs reduces the duration of flight bouts. Moreover, activity in the PAM neurons inhibits the GABAergic MBONs. Our data suggest that disinhibition of the identified neural circuit very likely occurs after flight initiation and is required to maintain the "flight state" when searching for distant sites, possibly related to food sources, mating partners, or a suitable egg-laying site. VIDEO ABSTRACT.

Flight motor networks modulate primary olfactory processing in the moth Manduca sexta

Nervous systems must distinguish sensory signals derived from an animal's own movements (reafference) from environmentally derived sources (exafference). To accomplish this, motor networks producing reafference transmit motor information, via a corollary discharge circuit (CDC), to affected sensory networks, modulating sensory function during behavior. While CDCs have been described in most sensory modalities, none have been observed projecting to an olfactory pathway. In moths, two mesothoracic to deutocerebral histaminergic neurons (MDHns) project from flight sensorimotor centers in the mesothoracic neuromere to the antennal lobe (AL), where they provide the sole source of histamine (HA), but whether they represent a CDC is unknown. We demonstrate that MDHn spiking activity is positively correlated with wing-motor output and increased before bouts of motor activity, suggesting that MDHns communicate global locomotor state, rather than providing a precisely timed motor copy. Within the AL, HA application sharpened entrainment of projection neuron responses to odor stimuli embedded within simulated wing-beat-induced flows, whereas MDHn axotomy or AL HA receptor (HA-r) blockade reduced entrainment. This finding is consistent with higher-order CDCs, as the MDHns enhanced rather than filtered entrainment of AL projection neurons. Finally, HA-r blockade increased odor detection and discrimination thresholds in behavior assays. These results establish MDHns as a CDC that modulates AL temporal resolution, enhancing odor-guided behavior. MDHns thus appear to represent a higher-order CDC to an insect olfactory pathway; this CDC's unique nature highlights the importance of motor-to-sensory signaling as a context-specific mechanism that fine-tunes sensory function.

Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

Insect flight is a complex behaviour that requires the integration of multiple sensory inputs with the flight motor output. Although previous genetic studies identified central brain monoaminergic neurons that modulate Drosophila flight, neuro-modulatory circuits underlying sustained flight bouts remain unexplored. Certain classes of dopaminergic and octopaminergic neurons are known to project to the Mushroom Body, a higher integrating centre in the insect brain, where based on contextual cues they modify neuronal output and thereby organismal behaviour. This study focuses on how monoaminergic modulation of Mushroom Body GABAergic output neurons regulates the duration of flight bouts. We demonstrate that flight inactivity is maintained by activity in specific Mushroom Body GABAergic output neurons. Longer flight bouts require inhibition of these neurons by activation of central dopaminergic neurons (Protocerebral Anterior Medial or PAM), resulting in disinhibition. Moreover, octopaminergic neurons in the sub-esophageal zone stimulate PAM neurons. Because similar neurons in the sub-esophageal zone are known to respond to hunger, food search is a likely contextual cue for disinhibition in the identified neural circuit.

Transient and Stable Chaos in Dipteran Flight Inspired Flapping Motion

This paper deals with the nonlinear fluid structure interaction (FSI) dynamics of a Dipteran flight motor inspired flapping system in an inviscid fluid. In the present study, the FSI effects are incorporated to an existing forced Duffing oscillator model to gain a clear understanding of the nonlinear dynamical behavior of the system in the presence of aerodynamic loads. The present FSI framework employs a potential flow solver to determine the aerodynamic loads and an explicit fourth-order Runge–Kutta scheme to solve the structural governing equations. A bifurcation analysis has been carried out considering the amplitude of the wing actuation force as the control parameter to investigate different complex states of the system. Interesting dynamical behavior including period doubling, chaotic transients, periodic windows, and finally an intermittent transition to stable chaotic attractor have been observed in the response with an increase in the bifurcation parameter. Similar dynamics is also reflected in the aerodynamic loads as well as in the trailing edge wake patterns.

Tyramine Actions on Drosophila Flight Behavior Are Affected by a Glial Dehydrogenase/Reductase.

The biogenic amines octopamine (OA) and tyramine (TA) modulate insect motor behavior in an antagonistic manner. OA generally enhances locomotor behaviors such as Drosophila larval crawling and flight, whereas TA decreases locomotor activity. However, the mechanisms and cellular targets of TA modulation of locomotor activity are incompletely understood. This study combines immunocytochemistry, genetics and flight behavioral assays in the Drosophila model system to test the role of a candidate enzyme for TA catabolism, named Nazgul (Naz), in flight motor behavioral control. We hypothesize that the dehydrogenase/reductase Naz represents a critical step in TA catabolism. Immunocytochemistry reveals that Naz is localized to a subset of Repo positive glial cells with cell bodies along the motor neuropil borders and numerous positive Naz arborizations extending into the synaptic flight motor neuropil. RNAi knock down of Naz in Repo positive glial cells reduces Naz protein level below detection level by Western blotting. The resulting consequence is a reduction in flight durations, thus mimicking known motor behavioral phenotypes as resulting from increased TA levels. In accord with the interpretation that reduced TA degradation by Naz results in increased TA levels in the flight motor neuropil, the motor behavioral phenotype can be rescued by blocking TA receptors. Our findings indicate that TA modulates flight motor behavior by acting on central circuitry and that TA is normally taken up from the central motor neuropil by Repo-positive glial cells, desaminated and further degraded by Naz.

Theoretical and practical investigation into the use of a bio-inspired “click” mechanism for the flight motor of a micro air vehicle

Recently, flapping wing micro air vehicles have received great attention with the drive to make smaller and smaller devices. This paper describes a theoretical investigation and subsequent practical implementation of a specific type of flight motor structure for this type of micro air vehicle that uses a “click” mechanism to improve mechanical efficiency. Diptera, which may use the mechanism, are the inspiration for this work. It builds on previous research into the “click” mechanism, which has been studied both from the biological and engineering points of view. It is difficult to capture the important fine details using a simple analytical model; hence, a multi-body dynamic software is used to model the device and to aid the design of a large-scale prototype. Force–deflection curves of the structure and the displacement response are obtained numerically and experimentally. The experimental and numerical results compare reasonably well, enabling the model to be used for further development and potential miniaturization of the flight motor structure. In a practical device, asymmetry occurs in the up- and down-stroke. The effects of this asymmetry are compared with previous results from analytical models. It is found that asymmetry offers a marginal improvement.