RESUMO
Insects constitute the most species-rich radiation of metazoa, a success that is 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 that are 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 three-dimensional motion of the wings with high-speed cameras. Using machine learning, 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 incorporating our hinge model generates flight manoeuvres 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.
Assuntos
Drosophila melanogaster , Voo Animal , Aprendizado de Máquina , Asas de Animais , Animais , Feminino , Fenômenos Biomecânicos/fisiologia , Drosophila melanogaster/fisiologia , Drosophila melanogaster/anatomia & histologia , Voo Animal/fisiologia , Músculos/fisiologia , Músculos/anatomia & histologia , Redes Neurais de Computação , Robótica , Asas de Animais/fisiologia , Asas de Animais/anatomia & histologia , Movimento/fisiologia , Cálcio/análise , Cálcio/metabolismoRESUMO
Motor neurons are the final common pathway1 through which the brain controls movement of the body, forming the basic elements from which all movement is composed. Yet how a single motor neuron contributes to control during natural movement remains unclear. Here we anatomically and functionally characterize the individual roles of the motor neurons that control head movement in the fly, Drosophila melanogaster. Counterintuitively, we find that activity in a single motor neuron rotates the head in different directions, depending on the starting posture of the head, such that the head converges towards a pose determined by the identity of the stimulated motor neuron. A feedback model predicts that this convergent behaviour results from motor neuron drive interacting with proprioceptive feedback. We identify and genetically2 suppress a single class of proprioceptive neuron3 that changes the motor neuron-induced convergence as predicted by the feedback model. These data suggest a framework for how the brain controls movements: instead of directly generating movement in a given direction by activating a fixed set of motor neurons, the brain controls movements by adding bias to a continuing proprioceptive-motor loop.
Assuntos
Drosophila melanogaster , Neurônios Motores , Movimento , Postura , Propriocepção , Animais , Drosophila melanogaster/anatomia & histologia , Drosophila melanogaster/genética , Drosophila melanogaster/fisiologia , Retroalimentação Fisiológica/fisiologia , Cabeça/fisiologia , Modelos Neurológicos , Neurônios Motores/fisiologia , Movimento/fisiologia , Postura/fisiologia , Propriocepção/genética , Propriocepção/fisiologia , MasculinoRESUMO
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 legs 1 , 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 wings 2 . 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 network 3 that accurately predicts wing motion from the activity of the steering muscles, and an encoder-decoder 4 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.
RESUMO
Our ability to sense and move our bodies relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Different subtypes of proprioceptors detect different kinematic features, such as joint position, movement, and vibration, but the mechanisms that underlie proprioceptor feature selectivity remain poorly understood. Using single-nucleus RNA sequencing (RNA-seq), we found that proprioceptor subtypes in the Drosophila leg lack differential expression of mechanosensitive ion channels. However, anatomical reconstruction of the proprioceptors and connected tendons revealed major biomechanical differences between subtypes. We built a model of the proprioceptors and tendons that identified a biomechanical mechanism for joint angle selectivity and predicted the existence of a topographic map of joint angle, which we confirmed using calcium imaging. Our findings suggest that biomechanical specialization is a key determinant of proprioceptor feature selectivity in Drosophila. More broadly, the discovery of proprioceptive maps reveals common organizational principles between proprioception and other topographically organized sensory systems.
Assuntos
Proteínas de Drosophila , Drosophila , Animais , Drosophila/metabolismo , Células Receptoras Sensoriais/fisiologia , Propriocepção/fisiologia , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Canais Iônicos/metabolismoRESUMO
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 function. 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 driver lines targeting 198 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. Taken together, the resources and results presented here form a powerful toolkit for future investigations of neural circuits and connectivity of premotor circuits while linking them to behavioral outputs.
RESUMO
Most animals have compound eyes, with tens to thousands of lenses attached rigidly to the exoskeleton. A natural assumption is that all of these species must resort to moving either their head or their body to actively change their visual input. However, classic anatomy has revealed that flies have muscles poised to move their retinas under the stable lenses of each compound eye1-3. Here we show that Drosophila use their retinal muscles to smoothly track visual motion, which helps to stabilize the retinal image, and also to perform small saccades when viewing a stationary scene. We show that when the retina moves, visual receptive fields shift accordingly, and that even the smallest retinal saccades activate visual neurons. Using a head-fixed behavioural paradigm, we find that Drosophila perform binocular, vergence movements of their retinas-which could enhance depth perception-when crossing gaps, and impairing the physiology of retinal motor neurons alters gap-crossing trajectories during free behaviour. That flies evolved an ability to actuate their retinas suggests that moving the eye independently of the head is broadly paramount for animals. The similarities of smooth and saccadic movements of the Drosophila retina and the vertebrate eye highlight a notable example of convergent evolution.
Assuntos
Drosophila , Movimentos Oculares , Músculos , Retina , Visão Ocular , Animais , Drosophila/fisiologia , Movimentos Oculares/fisiologia , Músculos/fisiologia , Retina/fisiologia , Movimentos Sacádicos/fisiologia , Visão Ocular/fisiologia , Visão Binocular , Percepção de Profundidade , Neurônios Motores , Cabeça/fisiologia , Drosophila melanogaster/fisiologia , Evolução BiológicaRESUMO
Animal wings deform during flight in ways that can enhance lift, facilitate flight control, and mitigate damage. Monitoring the structural and aerodynamic state of the wing is challenging because deformations are passive, and the flow fields are unsteady; it requires distributed mechanosensors that respond to local airflow and strain on the wing. Without a complete map of the sensor arrays, it is impossible to model control strategies underpinned by them. Here, we present the first systematic characterization of mechanosensors on the dragonfly's wings: morphology, distribution, and wiring. By combining a cross-species survey of sensor distribution with quantitative neuroanatomy and a high-fidelity finite element analysis, we show that the mechanosensors are well placed to perceive features of the wing dynamics relevant to flight. This work describes the wing sensory apparatus in its entirety and advances our understanding of the sensorimotor loop that facilitates exquisite flight control in animals with highly deformable wings.
RESUMO
In an elaborate form of inter-species exploitation, many insects hijack plant development to induce novel plant organs called galls that provide the insect with a source of nutrition and a temporary home. Galls result from dramatic reprogramming of plant cell biology driven by insect molecules, but the roles of specific insect molecules in gall development have not yet been determined. Here, we study the aphid Hormaphis cornu, which makes distinctive "cone" galls on leaves of witch hazel Hamamelis virginiana. We found that derived genetic variants in the aphid gene determinant of gall color (dgc) are associated with strong downregulation of dgc transcription in aphid salivary glands, upregulation in galls of seven genes involved in anthocyanin synthesis, and deposition of two red anthocyanins in galls. We hypothesize that aphids inject DGC protein into galls and that this results in differential expression of a small number of plant genes. dgc is a member of a large, diverse family of novel predicted secreted proteins characterized by a pair of widely spaced cysteine-tyrosine-cysteine (CYC) residues, which we named BICYCLE proteins. bicycle genes are most strongly expressed in the salivary glands specifically of galling aphid generations, suggesting that they may regulate many aspects of gall development. bicycle genes have experienced unusually frequent diversifying selection, consistent with their potential role controlling gall development in a molecular arms race between aphids and their host plants.
Assuntos
Afídeos/metabolismo , Hamamelis/parasitologia , Interações Hospedeiro-Parasita , Proteínas de Insetos/metabolismo , Tumores de Planta/parasitologia , Animais , Antocianinas/biossíntese , Afídeos/genética , Afídeos/patogenicidade , Feminino , Proteínas de Insetos/genética , Masculino , Folhas de Planta/parasitologiaRESUMO
Visually guided decision-making requires integration of information from distributed brain areas, necessitating a brain-wide approach to examine its neural mechanisms. New tools in Drosophila melanogaster enable circuits spanning the brain to be charted with single cell-type resolution. Here, we highlight recent advances uncovering the computations and circuits that transform and integrate visual information across the brain to make behavioral choices. Visual information flows from the optic lobes to three primary central brain regions: a sensorimotor mapping area and two 'higher' centers for memory or spatial orientation. Rapid decision-making during predator evasion emerges from the spike timing dynamics in parallel sensorimotor cascades. Goal-directed decisions may occur through memory, navigation and valence processing in the central complex and mushroom bodies.
Assuntos
Drosophila melanogaster , Drosophila , Animais , Encéfalo , Memória , Corpos PedunculadosRESUMO
We describe the anatomy of all the primary motor neurons in the fly proboscis and characterize their contributions to its diverse reaching movements. Pairing this behavior with the wealth of Drosophila's genetic tools offers the possibility to study motor control at single-neuron resolution, and soon throughout entire circuits. As an entry to these circuits, we provide detailed anatomy of proboscis motor neurons, muscles, and joints. We create a collection of fly strains to individually manipulate every proboscis muscle through control of its motor neurons, the first such collection for an appendage. We generate a model of the action of each proboscis joint, and find that only a small number of motor neurons are needed to produce proboscis reaching. Comprehensive control of each motor element in this numerically simple system paves the way for future study of both reflexive and flexible movements of this appendage.
Assuntos
Drosophila melanogaster/fisiologia , Neurônios Motores/fisiologia , Animais , Feminino , Masculino , Músculos/fisiologia , Reflexo/fisiologiaRESUMO
Drosophila melanogaster males perform a series of courtship behaviors that, when successful, result in copulation with a female. For over a century, mutations in the yellow gene, named for its effects on pigmentation, have been known to reduce male mating success. Prior work has suggested that yellow influences mating behavior through effects on wing extension, song, and/or courtship vigor. Here, we rule out these explanations, as well as effects on the nervous system more generally, and find instead that the effects of yellow on male mating success are mediated by its effects on pigmentation of male-specific leg structures called sex combs. Loss of yellow expression in these modified bristles reduces their melanization, which changes their structure and causes difficulty grasping females prior to copulation. These data illustrate why the mechanical properties of anatomy, not just neural circuitry, must be considered to fully understand the development and evolution of behavior.
Assuntos
Proteínas de Drosophila/genética , Drosophila melanogaster/genética , Preferência de Acasalamento Animal/fisiologia , Pigmentação/genética , Animais , Evolução Biológica , Fenômenos Biomecânicos , Copulação/fisiologia , Corte , Proteínas de Ligação a DNA/genética , Proteínas de Ligação a DNA/metabolismo , Proteínas de Drosophila/deficiência , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/anatomia & histologia , Drosophila melanogaster/metabolismo , Extremidades/anatomia & histologia , Feminino , Regulação da Expressão Gênica , Masculino , Proteínas do Tecido Nervoso/genética , Proteínas do Tecido Nervoso/metabolismo , Fatores de Transcrição/genética , Fatores de Transcrição/metabolismoRESUMO
Female behavior changes profoundly after mating. In Drosophila, the mechanisms underlying the long-term changes led by seminal products have been extensively studied. However, the effect of the sensory component of copulation on the female's internal state and behavior remains elusive. We pursued this question by dissociating the effect of coital sensory inputs from those of male ejaculate. We found that the sensory inputs of copulation cause a reduction of post-coital receptivity in females, referred to as the "copulation effect." We identified three layers of a neural circuit underlying this phenomenon. Abdominal neurons expressing the mechanosensory channel Piezo convey the signal of copulation to female-specific ascending neurons, LSANs, in the ventral nerve cord. LSANs relay this information to neurons expressing myoinhibitory peptides in the brain. We hereby provide a neural mechanism by which the experience of copulation facilitates females encoding their mating status, thus adjusting behavior to optimize reproduction.
Assuntos
Encéfalo/metabolismo , Copulação/fisiologia , Proteínas de Drosophila/metabolismo , Canais Iônicos/metabolismo , Mecanotransdução Celular/fisiologia , Neurônios/metabolismo , Abdome , Animais , Encéfalo/fisiologia , Proteínas de Drosophila/fisiologia , Drosophila melanogaster , Feminino , Gânglios Sensitivos/metabolismo , Gânglios Sensitivos/fisiologia , Canais Iônicos/fisiologia , Vias Neurais , Neurônios/fisiologia , Comportamento Sexual Animal/fisiologiaRESUMO
Jumping in planthopper and froghopper insects is propelled by a catapult-like mechanism requiring mechanical storage of energy and its quick release to accelerate the hind legs rapidly. To understand the functional biomechanics involved in these challenging movements, the internal skeleton, tendons and muscles involved were reconstructed in 3-D from confocal scans in unprecedented detail. Energy to power jumping was generated by slow contractions of hind leg depressor muscles and then stored by bending specialised elements of the thoracic skeleton that are composites of the rubbery protein resilin sandwiched between layers of harder cuticle with air-filled tunnels reducing mass. The images showed that the lever arm of the power-producing muscle changed in magnitude during jumping, but at all joint angles would cause depression, suggesting a mechanism by which the stored energy is released. This methodological approach illuminates how miniaturized components interact and function in complex and rapid movements of small animals.
Assuntos
Fenômenos Biomecânicos , Metabolismo Energético , Hemípteros/fisiologia , Locomoção , Músculos/fisiologia , Esqueleto/fisiologia , Tendões/fisiologia , Animais , Imageamento Tridimensional , Microscopia Confocal , Modelos BiológicosRESUMO
The amphipod crustacean Parhyale hawaiensis is a blossoming model system for studies of developmental mechanisms and more recently regeneration. We have sequenced the genome allowing annotation of all key signaling pathways, transcription factors, and non-coding RNAs that will enhance ongoing functional studies. Parhyale is a member of the Malacostraca clade, which includes crustacean food crop species. We analysed the immunity related genes of Parhyale as an important comparative system for these species, where immunity related aquaculture problems have increased as farming has intensified. We also find that Parhyale and other species within Multicrustacea contain the enzyme sets necessary to perform lignocellulose digestion ('wood eating'), suggesting this ability may predate the diversification of this lineage. Our data provide an essential resource for further development of Parhyale as an experimental model. The first malacostracan genome will underpin ongoing comparative work in food crop species and research investigating lignocellulose as an energy source.
Assuntos
Anfípodes/genética , Proteínas de Artrópodes/genética , Genoma , Estágios do Ciclo de Vida/genética , Lignina/metabolismo , Redes e Vias Metabólicas/genética , Anfípodes/classificação , Anfípodes/crescimento & desenvolvimento , Anfípodes/metabolismo , Animais , Aquicultura , Proteínas de Artrópodes/imunologia , Feminino , Regulação da Expressão Gênica no Desenvolvimento , Ontologia Genética , Sequenciamento de Nucleotídeos em Larga Escala , Imunidade Inata , Cariótipo , Estágios do Ciclo de Vida/imunologia , Masculino , Redes e Vias Metabólicas/imunologia , Anotação de Sequência Molecular , Filogenia , RNA não Traduzido/genética , RNA não Traduzido/imunologia , Regeneração , Transdução de Sinais , Fatores de Transcrição/genética , Fatores de Transcrição/imunologiaRESUMO
Motivation controls behavior [1]. A variety of food-related behaviors undergo motivational modulation by hunger, satiety, and other states [2-4]. Here we searched for critical satiation factors modulating approach to an odor associated with sugar reward in Drosophila melanogaster. We selectively manipulated different parameters associated with feeding, such as internal glucose levels, and determined which are required for suppressing conditioned odor approach. Surprisingly, glucose levels in the hemolymph, nutritional value, sweetness of the food, and ingested volume (above a minimal threshold) did not influence behavior suppression. Instead, we found that the total osmolarity of ingested food is a critical satiation factor. In parallel, we found that conditioned approach is transiently suppressed by artificial stimulation of adipokinetic hormone (AKH) expressing corpora cardiaca cells, which causes elevation of hemolymph carbohydrate and lipid concentrations [5, 6]. This result implies that a rise in hemolymph osmolarity, without the experience of feeding, is sufficient to satiate conditioned odor approach. AKH stimulation did not affect innate sugar preference, suggesting that multiple satiation signals control different sets of appetitive behaviors.
Assuntos
Drosophila melanogaster/fisiologia , Animais , Condicionamento Clássico , Comportamento Alimentar , Feminino , Glucose/fisiologia , Hormônios de Inseto/metabolismo , Masculino , Motivação , Sistemas Neurossecretores/metabolismo , Valor Nutritivo , Percepção Olfatória , Oligopeptídeos/metabolismo , Ácido Pirrolidonocarboxílico/análogos & derivados , Ácido Pirrolidonocarboxílico/metabolismo , Recompensa , Percepção GustatóriaRESUMO
Animals approach stimuli that predict a pleasant outcome. After the paired presentation of an odour and a reward, Drosophila melanogaster can develop a conditioned approach towards that odour. Despite recent advances in understanding the neural circuits for associative memory and appetitive motivation, the cellular mechanisms for reward processing in the fly brain are unknown. Here we show that a group of dopamine neurons in the protocerebral anterior medial (PAM) cluster signals sugar reward by transient activation and inactivation of target neurons in intact behaving flies. These dopamine neurons are selectively required for the reinforcing property of, but not a reflexive response to, the sugar stimulus. In vivo calcium imaging revealed that these neurons are activated by sugar ingestion and the activation is increased on starvation. The output sites of the PAM neurons are mainly localized to the medial lobes of the mushroom bodies (MBs), where appetitive olfactory associative memory is formed. We therefore propose that the PAM cluster neurons endow a positive predictive value to the odour in the MBs. Dopamine in insects is known to mediate aversive reinforcement signals. Our results highlight the cellular specificity underlying the various roles of dopamine and the importance of spatially segregated local circuits within the MBs.
Assuntos
Neurônios Dopaminérgicos/fisiologia , Drosophila melanogaster/citologia , Drosophila melanogaster/fisiologia , Memória/fisiologia , Odorantes/análise , Recompensa , Animais , Comportamento Apetitivo/fisiologia , Sinalização do Cálcio , Dendritos/fisiologia , Dopamina/metabolismo , Neurônios Dopaminérgicos/citologia , Corpos Pedunculados/citologia , Corpos Pedunculados/metabolismo , Olfato/genética , Olfato/fisiologiaRESUMO
Animals acquire predictive values of sensory stimuli through reinforcement. In the brain of Drosophila melanogaster, activation of two types of dopamine neurons in the PAM and PPL1 clusters has been shown to induce aversive odor memory. Here, we identified the third cell type and characterized aversive memories induced by these dopamine neurons. These three dopamine pathways all project to the mushroom body but terminate in the spatially segregated subdomains. To understand the functional difference of these dopamine pathways in electric shock reinforcement, we blocked each one of them during memory acquisition. We found that all three pathways partially contribute to electric shock memory. Notably, the memories mediated by these neurons differed in temporal stability. Furthermore, combinatorial activation of two of these pathways revealed significant interaction of individual memory components rather than their simple summation. These results cast light on a cellular mechanism by which a noxious event induces different dopamine signals to a single brain structure to synthesize an aversive memory.
Assuntos
Dopamina , Drosophila melanogaster , Memória/fisiologia , Corpos Pedunculados , Odorantes , Animais , Dopamina/genética , Dopamina/metabolismo , Dopamina/fisiologia , Neurônios Dopaminérgicos/metabolismo , Neurônios Dopaminérgicos/fisiologia , Proteínas de Drosophila/genética , Proteínas de Drosophila/metabolismo , Proteínas de Drosophila/fisiologia , Drosophila melanogaster/genética , Drosophila melanogaster/fisiologia , Estimulação Elétrica , Canais Iônicos , Corpos Pedunculados/metabolismo , Corpos Pedunculados/fisiologia , Transdução de Sinais/genética , Transdução de Sinais/fisiologia , Canal de Cátion TRPA1 , Canais de Cátion TRPC/genética , Canais de Cátion TRPC/fisiologia , Fatores de Transcrição/genética , Fatores de Transcrição/metabolismo , Fatores de Transcrição/fisiologiaRESUMO
A fundamental duty of any efficient memory system is to prevent long-lasting storage of poorly relevant information. However, little is known about dedicated mechanisms that appropriately trigger production of long-term memory (LTM). We examined the role of Drosophila dopaminergic neurons in the control of LTM formation and found that they act as a switch between two exclusive consolidation pathways leading to LTM or anesthesia-resistant memory (ARM). Blockade, after aversive olfactory conditioning, of three pairs of dopaminergic neurons projecting on mushroom bodies, the olfactory memory center, enhanced ARM, whereas their overactivation conversely impaired ARM. Notably, blockade of these neurons during the intertrial intervals of a spaced training precluded LTM formation. Two pairs of these dopaminergic neurons displayed sustained calcium oscillations in naive flies. Oscillations were weakened by ARM-inducing massed training and were enhanced during LTM formation. Our results indicate that oscillations of two pairs of dopaminergic neurons control ARM levels and gate LTM.
Assuntos
Sinalização do Cálcio/fisiologia , Neurônios Dopaminérgicos/fisiologia , Memória de Longo Prazo/fisiologia , Corpos Pedunculados/fisiologia , Animais , Animais Geneticamente Modificados , Drosophila melanogaster , Feminino , Fatores de TempoRESUMO
Aversive olfactory memory is formed in the mushroom bodies in Drosophila melanogaster. Memory retrieval requires mushroom body output, but the manner in which a memory trace in the mushroom body drives conditioned avoidance of a learned odor remains unknown. To identify neurons that are involved in olfactory memory retrieval, we performed an anatomical and functional screen of defined sets of mushroom body output neurons. We found that MB-V2 neurons were essential for retrieval of both short- and long-lasting memory, but not for memory formation or memory consolidation. MB-V2 neurons are cholinergic efferent neurons that project from the mushroom body vertical lobes to the middle superiormedial protocerebrum and the lateral horn. Notably, the odor response of MB-V2 neurons was modified after conditioning. As the lateral horn has been implicated in innate responses to repellent odorants, we propose that MB-V2 neurons recruit the olfactory pathway involved in innate odor avoidance during memory retrieval.