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Spatial memory helps animals to navigate familiar environments. In insects, spatial memory has extensively been studied in central place foragers such as ants and bees. However, if butterflies memorize a spatial location remains unclear. Here, we conducted behavioural experiments to test whether monarch butterflies (Danaus plexippus) can remember and retrieve the spatial location of a food source. We placed several visually identical feeders in a flight cage, with only one feeder providing sucrose solution. Across multiple days, individual butterflies predominantly visited the rewarding feeder. Next, we displaced a salient landmark close to the feeders to test which visual cue the butterflies used to relocate the rewarding feeder. While occasional landmark displacements were ignored by the butterflies and did not affect their decisions, systematic displacement of both the landmark and the rewarding feeder demonstrated that the butterflies associated the salient landmark with the feeder's position. Altogether, we show that butterflies consolidate and retrieve spatial memory in the context of foraging.
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Borboletas , Abelhas , Animais , Memória Espacial , AlimentosRESUMO
Neural processing of a desired moving direction requires the continuous comparison between the current heading and the goal direction. While the neural basis underlying the current heading is well-studied, the coding of the goal direction remains unclear in insects. Here, we used tetrode recordings in tethered flying monarch butterflies to unravel how a goal direction is represented in the insect brain. While recording, the butterflies maintained robust goal directions relative to a virtual sun. By resetting their goal directions, we found neurons whose spatial tuning was tightly linked to the goal directions. Importantly, their tuning was unaffected when the butterflies changed their heading after compass perturbations, showing that these neurons specifically encode the goal direction. Overall, we here discovered invertebrate goal-direction neurons that share functional similarities to goal-direction cells reported in mammals. Our results give insights into the evolutionarily conserved principles of goal-directed spatial orientation in animals.
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Borboletas , Animais , Objetivos , Encéfalo , Neurônios , Orientação Espacial , MamíferosRESUMO
Monarch butterflies (Danaus plexippus) have become a superb model system to unravel how the tiny insect brain controls an impressive navigation behavior, such as long-distance migration. Moreover, the ability to compare the neural substrate between migratory and nonmigratory Monarch butterflies provides us with an attractive model to specifically study how the insect brain is adapted for migration. We here review our current progress on the neural substrate of spatial orientation in Monarch butterflies and how their spectacular annual migration might be controlled by their brain. We also discuss open research questions, the answers to which will provide important missing pieces to obtain a full picture of insect migration - from the perception of orientation cues to the neural control of migration.
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Borboletas , Animais , Migração Animal , Encéfalo , Sinais (Psicologia) , Modelos BiológicosRESUMO
The central complex is a brain region in the insect brain that houses a neural network specialized to encode directional information. Directional coding has traditionally been investigated with compass cues that revolve in full rotations and at constant angular velocities around the insect's head. However, these stimulus conditions do not fully simulate an insect's sensory perception of compass cues during navigation. In nature, an insect flight is characterized by abrupt changes in moving direction as well as constant changes in velocity. The influence of such varying cue dynamics on compass coding remains unclear. We performed long-term tetrode recordings from the brain of monarch butterflies to study how central complex neurons respond to different stimulus velocities and directions. As these butterflies derive directional information from the sun during migration, we measured the neural response to a virtual sun. The virtual sun was either presented as a spot that appeared at random angular positions or was rotated around the butterfly at different angular velocities and directions. By specifically manipulating the stimulus velocity and trajectory, we dissociated the influence of angular velocity and direction on compass coding. While the angular velocity substantially affected the tuning directedness, the stimulus trajectory influenced the shape of the angular tuning curve. Taken together, our results suggest that the central complex flexibly adjusts its directional coding to the current stimulus dynamics ensuring a precise compass even under highly demanding conditions such as during rapid flight maneuvers.
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Borboletas , Animais , Borboletas/fisiologia , Encéfalo/fisiologia , Cabeça , Interneurônios , SensaçãoRESUMO
Ball rolling dung beetles use a wide range of cues to steer themselves along a fixed bearing, including the spectral gradient of scattered skylight that spans the sky. Here, we define the spectral sensitivity of the diurnal dung beetle Kheper lamarcki and use the information to explore the orientation performance under a range of spectral light combinations. We find that, when presented with spectrally diverse stimuli, the beetles primarily orient to the apparent brightness differences as perceived by their green photoreceptors. Under certain wavelength combinations, they also rely on spectral information to guide their movements, but the brightness and spectral directional information is never fully disentangled. Overall, our results suggest the use of a dichromatic, primitive colour vision system for the extraction of directional information from the celestial spectral gradient to support straight-line orientation. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.
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Artrópodes , Besouros , Animais , Besouros/fisiologia , Sinais (Psicologia) , Fezes , NeurôniosRESUMO
Monarch butterflies rely on external cues for orientation during their annual long-distance migration from Northern US and Canada to Central Mexico. These external cues can be celestial cues, such as the sun or polarized light, which are processed in a brain region termed the central complex (CX). Previous research typically focused on how individual simulated celestial cues are encoded in the butterfly's CX. However, in nature, the butterflies perceive several celestial cues at the same time and need to integrate them to effectively use the compound of all cues for orientation. In addition, a recent behavioral study revealed that monarch butterflies can rely on terrestrial cues, such as the panoramic skyline, for orientation and use them in combination with the sun to maintain a directed flight course. How the CX encodes a combination of celestial and terrestrial cues and how they are weighted in the butterfly's CX is still unknown. Here, we examined how input neurons of the CX, termed TL neurons, combine celestial and terrestrial information. While recording intracellularly from the neurons, we presented a sun stimulus and polarized light to the butterflies as well as a simulated sun and a panoramic scene simultaneously. Our results show that celestial cues are integrated linearly in these cells, while the combination of the sun and a panoramic skyline did not always follow a linear integration of action potential rates. Interestingly, while the sun and polarized light were invariantly weighted between individual neurons, the sun stimulus and panoramic skyline were dynamically weighted when both stimuli were simultaneously presented. Taken together, this dynamic weighting between celestial and terrestrial cues may allow the butterflies to flexibly set their cue preference during navigation.
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Borboletas , Potenciais de Ação/fisiologia , Animais , Encéfalo/fisiologia , Sinais (Psicologia) , Neurônios/fisiologiaRESUMO
Multisensory integration plays a central role in perception, as all behaviors usually require the input of different sensory signals. For instance, for a foraging honeybee the association of a food source includes the combination of olfactory and visual cues to be categorized as a flower. Moreover, homing after successful foraging using celestial cues and the panoramic scenery may be dominated by visual cues. Hence, dependent on the context, one modality might be leading and influence the processing of other modalities. To unravel the complex neural mechanisms behind this process we studied honeybee mushroom body output neurons (MBON). MBONs represent the first processing level after olfactory-visual convergence in the honeybee brain. This was physiologically confirmed in our previous study by characterizing a subpopulation of multisensory MBONs. These neurons categorize incoming sensory inputs into olfactory, visual, and olfactory-visual information. However, in addition to multisensory units a prominent population of MBONs was sensitive to visual cues only. Therefore, we asked which visual features might be represented at this high-order integration level. Using extracellular, multi-unit recordings in combination with visual and olfactory stimulation, we separated MBONs with multisensory responses from purely visually driven MBONs. Further analysis revealed, for the first time, that visually driven MBONs of both groups encode detailed aspects within this individual modality, such as light intensity and light identity. Moreover, we show that these features are separated by different MBON subpopulations, for example by extracting information about brightness and wavelength. Most interestingly, the latter MBON population was tuned to separate UV-light from other light stimuli, which were only poorly differentiated from each other. A third MBON subpopulation was neither tuned to brightness nor to wavelength and encoded the general presence of light. Taken together, our results support the view that the mushroom body, a high-order sensory integration, learning and memory center in the insect brain, categorizes sensory information by separating different behaviorally relevant aspects of the multisensory scenery and that these categories are channeled into distinct MBON subpopulations.
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Insects are well known for their ability to keep track of their heading direction based on a combination of skylight cues and visual landmarks. This allows them to navigate back to their nest, disperse throughout unfamiliar environments, as well as migrate over large distances between their breeding and non-breeding habitats. The monarch butterfly (Danaus plexippus), for instance, is known for its annual southward migration from North America to certain trees in Central Mexico. To maintain a constant flight route, these butterflies use a time-compensated sun compass, which is processed in a region in the brain, termed the central complex. However, to successfully complete their journey, the butterflies' brain must generate a multitude of orientation strategies, allowing them to dynamically switch from sun-compass orientation to a tactic behavior toward a certain target. To study whether monarch butterflies exhibit different orientation modes and if they can switch between them, we observed the orientation behavior of tethered flying butterflies in a flight simulator while presenting different visual cues to them. We found that the butterflies' behavior depended on the presented visual stimulus. Thus, while a dark stripe was used for flight stabilization, a bright stripe was fixated by the butterflies in their frontal visual field. If we replaced a bright stripe with a simulated sun stimulus, the butterflies switched their behavior and exhibited compass orientation. Taken together, our data show that monarch butterflies rely on and switch between different orientation modes, allowing the animal to adjust orientation to its actual behavioral demands.
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Borboletas , Migração Animal , Animais , Encéfalo , Sinais (Psicologia) , Melhoramento VegetalRESUMO
For navigation, animals use a robust internal compass. Compass navigation is crucial for long-distance migrating animals like monarch butterflies, which use the sun to navigate over 4,000 km to their overwintering sites every fall. Sun-compass neurons of the central complex have only been recorded in immobile butterflies, and experimental evidence for encoding the animal's heading in these neurons is still missing. Although the activity of central-complex neurons exhibits a locomotor-dependent modulation in many insects, the function of such modulations remains unexplored. Here, we developed tetrode recordings from tethered flying monarch butterflies to reveal how flight modulates heading representation. We found that, during flight, heading-direction neurons change their tuning, transforming the central-complex network to function as a global compass. This compass is characterized by the dominance of processing steering feedback and allows for robust heading representation even under unreliable visual scenarios, an ideal strategy for maintaining a migratory heading over enormous distances.
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Borboletas , Migração Animal/fisiologia , Animais , Borboletas/fisiologia , Neurônios/fisiologiaRESUMO
Insect neuroscience generates vast amounts of highly diverse data, of which only a small fraction are findable, accessible and reusable. To promote an open data culture, we have therefore developed the InsectBrainDatabase (IBdb), a free online platform for insect neuroanatomical and functional data. The IBdb facilitates biological insight by enabling effective cross-species comparisons, by linking neural structure with function, and by serving as general information hub for insect neuroscience. The IBdb allows users to not only effectively locate and visualize data, but to make them widely available for easy, automated reuse via an application programming interface. A unique private mode of the database expands the IBdb functionality beyond public data deposition, additionally providing the means for managing, visualizing, and sharing of unpublished data. This dual function creates an incentive for data contribution early in data management workflows and eliminates the additional effort normally associated with publicly depositing research data.
Insect neuroscience, like any field in the natural sciences, generates vast amounts of data. Currently, only a fraction are publicly available, and even less are reusable. This is because insect neuroscience data come in many formats and from many species. Some experiments focus on what insect brains look like (morphology), while others focus on how insect brains work (function). Some data come in the form of high-speed video, while other data contain voltage traces from individual neurons. Sharing is not as simple as uploading the raw files to the internet. To get a clear picture of how insect brains work, researchers need a way to cross-reference and connect different experiments. But, as it stands, there is no dedicated place for insect neuroscientists to share and explore such a diverse body of work. The community needs an open data repository that can link different types of data across many species, and can evolve as more data become available. Above all, this repository needs to be easy for researchers to use. To meet these specifications, Heinze et al. developed the Insect Brain Database. The database organizes data into three categories: species, brain structures, and neuron types. Within these categories, each entry has its own profile page. These pages bring different experiments together under one heading, allowing researchers to combine and compare data of different types. As researchers add more experiments, the profile pages will grow and evolve. To make the data easy to navigate, Heinze et al. developed a visual search tool. A combination of 2D and 3D images allow users to explore the data by anatomical location, without the need for expert knowledge. Researchers also have the option to upload their work in private mode, allowing them to securely share unpublished data. The Insect Brain Database brings data together in a way that is accessible not only to researchers, but also to students, and non-scientists. It will help researchers to find related work, to reuse existing data, and to build an open data culture. This has the potential to drive new discoveries combining research across the whole of the insect neuroscience field.
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Pesquisa Biomédica , Encéfalo/fisiologia , Bases de Dados Factuais , Gestão da Informação , Armazenamento e Recuperação da Informação , Insetos/fisiologia , Fenômenos Fisiológicos do Sistema Nervoso , Neurociências , Animais , Encéfalo/anatomia & histologia , Gráficos por Computador , Mineração de Dados , Insetos/anatomia & histologia , Internet , Interface Usuário-ComputadorRESUMO
In recent years, bumblebees have become a prominent insect model organism for a variety of biological disciplines, particularly to investigate learning behaviors as well as visual performance. Understanding these behaviors and their underlying neurobiological principles requires a clear understanding of brain anatomy. Furthermore, to be able to compare neuronal branching patterns across individuals, a common framework is required, which has led to the development of 3D standard brain atlases in most of the neurobiological insect model species. Yet, no bumblebee 3D standard brain atlas has been generated. Here we present a brain atlas for the buff-tailed bumblebee Bombus terrestris using micro-computed tomography (micro-CT) scans as a source for the raw data sets, rather than traditional confocal microscopy, to produce the first ever micro-CT-based insect brain atlas. We illustrate the advantages of the micro-CT technique, namely, identical native resolution in the three cardinal planes and 3D structure being better preserved. Our Bombus terrestris brain atlas consists of 30 neuropils reconstructed from ten individual worker bees, with micro-CT allowing us to segment neuropils completely intact, including the lamina, which is a tissue structure often damaged when dissecting for immunolabeling. Our brain atlas can serve as a platform to facilitate future neuroscience studies in bumblebees and illustrates the advantages of micro-CT for specific applications in insect neuroanatomy.
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Encéfalo/diagnóstico por imagem , Tomografia Computadorizada por Raios X/métodos , Animais , AbelhasRESUMO
Every autumn, monarch butterflies migrate from North America to their overwintering sites in Central Mexico. To maintain their southward direction, these butterflies rely on celestial cues as orientation references. The position of the sun combined with additional skylight cues are integrated in the central complex, a region in the butterfly's brain that acts as an internal compass. However, the central complex does not solely guide the butterflies on their migration but also helps monarchs in their non-migratory form manoeuvre on foraging trips through their habitat. By comparing the activity of input neurons of the central complex between migratory and non-migratory butterflies, we investigated how a different lifestyle affects the coding of orientation information in the brain. During recording, we presented the animals with different simulated celestial cues and found that the encoding of the sun was narrower in migratory compared to non-migratory butterflies. This feature might reflect the need of the migratory monarchs to rely on a precise sun compass to keep their direction during their journey. Taken together, our study sheds light on the neural coding of celestial cues and provides insights into how a compass is adapted in migratory animals to successfully steer them to their destination.
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Borboletas , Migração Animal , Animais , México , Neurônios , América do NorteRESUMO
Distant and predictable features in the environment make ideal compass cues to allow movement along a straight path. Ball-rolling dung beetles use a wide range of different signals in the day or night sky to steer themselves along a fixed bearing. These include the sun, the Milky Way, and the polarization pattern generated by the moon. Almost two decades of research into these remarkable creatures have shown that the dung beetle's compass is flexible and readily adapts to the cues available in its current surroundings. In the morning and afternoon, dung beetles use the sun to orient, but at midday, they prefer to use the wind, and at night or in a forest, they rely primarily on polarized skylight to maintain straight paths. We are just starting to understand the neuronal substrate underlying the dung beetle's compass and the mystery of why these beetles start each journey with a dance.
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Besouros/fisiologia , Orientação Espacial , Navegação Espacial , Animais , Encéfalo/fisiologiaRESUMO
Unusual amongst dung beetles, Scarabaeus galenus digs a burrow that it provisions by making repeated trips to a nearby dung pile. Even more remarkable is that these beetles return home moving backwards, with a pellet of dung between their hind legs. Here, we explore the strategy that S. galenus uses to find its way home. We find that, like many other insects, they use path integration to calculate the direction and distance to their home. If they fail to locate their burrow, the beetles initiate a distinct looping search behaviour that starts with a characteristic sharp turn, we have called a 'turning point'. When homing beetles are passively displaced or transferred to an unfamiliar environment, they initiate a search at a point very close to the location of their fictive burrow-that is, a spot at the same relative distance and direction from the pick-up point as the original burrow. Unlike other insects, S. galenus do not appear to supplement estimates of the burrow location with landmark information. Thus, S. galenus represents a rare case of a consistently backward-homing animal that does not use landmarks to augment its path integration strategy.
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Besouros , Animais , Comportamento Animal , Sinais (Psicologia) , Fezes , InsetosRESUMO
Monarch butterflies (Danaus plexippus) are prominent for their annual long-distance migration from North America to their overwintering area in Central Mexico. To find their way on this long journey, they use a sun compass as their main orientation reference but will also adjust their migratory direction with respect to mountain ranges. This indicates that the migratory butterflies also attend to the panorama to guide their travels. Although the compass has been studied in detail in migrating butterflies, little is known about the orientation abilities of non-migrating butterflies. Here, we investigated whether non-migrating butterflies - which stay in a more restricted area to feed and breed - also use a similar compass system to guide their flights. Performing behavioral experiments on tethered flying butterflies in an indoor LED flight simulator, we found that the monarchs fly along straight tracks with respect to a simulated sun. When a panoramic skyline was presented as the only orientation cue, the butterflies maintained their flight direction only during short sequences, suggesting that they potentially use it for flight stabilization. We further found that when we presented the two cues together, the butterflies incorporate both cues in their compass. Taken together, we show here that non-migrating monarch butterflies can combine multiple visual cues for robust orientation, an ability that may also aid them during their migration.
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Borboletas , Migração Animal , Animais , Sinais (Psicologia) , México , América do Norte , Orientação EspacialRESUMO
Cataglyphis ants are known for their outstanding navigational abilities. They return to their inconspicuous nest after far-reaching foraging trips using path integration, and whenever available, learn and memorize visual features of panoramic sceneries. To achieve this, the ants combine directional visual information from celestial cues and panoramic scenes with distance information from an intrinsic odometer. The largely vision-based navigation in Cataglyphis requires sophisticated neuronal networks to process the broad repertoire of visual stimuli. Although Cataglyphis ants have been subjected to many neuroethological studies, little is known about the general neuronal organization of their central brain and the visual pathways beyond major circuits. Here, we provide a comprehensive, three-dimensional neuronal map of synapse-rich neuropils in the brain of Cataglyphis nodus including major connecting fiber systems. In addition, we examined neuronal tracts underlying the processing of visual information in more detail. This study revealed a total of 33 brain neuropils and 30 neuronal fiber tracts including six distinct tracts between the optic lobes and the cerebrum. We also discuss the importance of comparative studies on insect brain architecture for a profound understanding of neuronal networks and their function.
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Formigas/anatomia & histologia , Formigas/fisiologia , Encéfalo/anatomia & histologia , Navegação Espacial/fisiologia , Vias Visuais/anatomia & histologia , Animais , Encéfalo/fisiologia , Imuno-Histoquímica , Aprendizagem/fisiologia , Microscopia Confocal , Neurônios/citologia , Neurônios/fisiologia , Neurópilo/citologia , Neurópilo/fisiologia , Vias Visuais/fisiologia , Percepção Visual/fisiologiaRESUMO
Nasonia, a genus of parasitoid wasps, is a promising model system in the study of developmental and evolutionary genetics, as well as complex traits such as learning. Of these "jewel wasps", the species Nasonia vitripennis is widely spread and widely studied. To accelerate neuroscientific research in this model species, fundamental knowledge of its nervous system is needed. To this end, we present an average standard brain of recently eclosed naïve female N. vitripennis wasps obtained by the iterative shape averaging method. This "Jewel Wasp Standard Brain" includes the optic lobe (excluding the lamina), the anterior optic tubercle, the antennal lobe, the lateral horn, the mushroom body, the central complex, and the remaining unclassified neuropils in the central brain. Furthermore, we briefly describe these well-defined neuropils and their subregions in the N. vitripennis brain. A volumetric analysis of these neuropils is discussed in the context of brains of other insect species. The Jewel Wasp Standard Brain will provide a framework to integrate and consolidate the results of future neurobiological studies in N. vitripennis. In addition, the volumetric analysis provides a baseline for future work on age- and experience-dependent brain plasticity.
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Vespas/anatomia & histologia , Animais , Encéfalo/anatomia & histologia , Encéfalo/citologia , Feminino , Neurópilo/citologiaRESUMO
South African ball-rolling dung beetles exhibit a unique orientation behavior to avoid competition for food: after forming a piece of dung into a ball, they efficiently escape with it from the dung pile along a straight-line path. To keep track of their heading, these animals use celestial cues, such as the sun, as an orientation reference. Here we show that wind can also be used as a guiding cue for the ball-rolling beetles. We demonstrate that this mechanosensory compass cue is only used when skylight cues are difficult to read, i.e., when the sun is close to the zenith. This raises the question of how the beetles combine multimodal orientation input to obtain a robust heading estimate. To study this, we performed behavioral experiments in a tightly controlled indoor arena. This revealed that the beetles register directional information provided by the sun and the wind and can use them in a weighted manner. Moreover, the directional information can be transferred between these 2 sensory modalities, suggesting that they are combined in the spatial memory network in the beetle's brain. This flexible use of compass cue preferences relative to the prevailing visual and mechanosensory scenery provides a simple, yet effective, mechanism for enabling precise compass orientation at any time of the day.