| 1. |
- de Vries, Liv, et al.
(författare)
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Comparison of Navigation-Related Brain Regions in Migratory versus Non-Migratory Noctuid Moths
- 2017
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Ingår i: Frontiers in Behavioral Neuroscience. - : Frontiers Media SA. - 1662-5153. ; 11
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Tidskriftsartikel (refereegranskat)abstract
- Brain structure and function are tightly correlated across all animals. While these relations are ultimately manifestations of differently wired neurons, many changes in neural circuit architecture lead to larger-scale alterations visible already at the level of brain regions. Locating such differences has served as a beacon for identifying brain areas that are strongly associated with the ecological needs of a species—thus guiding the way towards more detailed investigations of how brains underlie species-specific behaviors. Particularly in relation to sensory requirements, volume-differences in neural tissue between closely related species reflect evolutionary investments that correspond to sensory abilities. Likewise, memory-demands imposed by lifestyle have revealed similar adaptations in regions associated with learning. Whether this is also the case for species that differ in their navigational strategy is currently unknown. While the brain regions associated with navigational control in insects have been identified (central complex (CX), lateral complex (LX) and anterior optic tubercles (AOTU)), it remains unknown in what way evolutionary investments have been made to accommodate particularly demanding navigational strategies. We have thus generated average-shape atlases of navigation-related brain regions of a migratory and a non-migratory noctuid moth and used volumetric analysis to identify differences. We further compared the results to identical data from Monarch butterflies. Whereas we found differences in the size of the nodular unit of the AOTU, the LX and the protocerebral bridge (PB) between the two moths, these did not unambiguously reflect migratory behavior across all three species. We conclude that navigational strategy, at least in the case of long-distance migration in lepidopteran insects, is not easily deductible from overall neuropil anatomy. This suggests that the adaptations needed to ensure successful migratory behavior are found in the detailed wiring characteristics of the neural circuits underlying navigation—differences that are only accessible through detailed physiological and ultrastructural investigations. The presented results aid this task in two ways. First, the identified differences in neuropil volumes serve as promising initial targets for electrophysiology. Second, the new standard atlases provide an anatomical reference frame for embedding all functional data obtained from the brains of the Bogong and the Turnip moth.
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| 2. |
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| 4. |
- Heinze, Stanley, et al.
(författare)
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Principles of Insect Path Integration
- 2018
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Ingår i: Current Biology. - : Elsevier BV. - 0960-9822. ; 28:17, s. 1043-1058
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Forskningsöversikt (refereegranskat)abstract
- Continuously monitoring its position in space relative to a goal is one of the most essential tasks for an animal that moves through its environment. Species as diverse as rats, bees, and crabs achieve this by integrating all changes of direction with the distance covered during their foraging trips, a process called path integration. They generate an estimate of their current position relative to a starting point, enabling a straight-line return, following what is known as a home vector. While in theory path integration always leads the animal precisely back home, in the real world noise limits the usefulness of this strategy when operating in isolation. Noise results from stochastic processes in the nervous system and from unreliable sensory information, particularly when obtaining heading estimates. Path integration, during which angular self-motion provides the sole input for encoding heading (idiothetic path integration), results in accumulating errors that render this strategy useless over long distances. In contrast, when using an external compass this limitation is avoided (allothetic path integration). Many navigating insects indeed rely on external compass cues for estimating body orientation, whereas they obtain distance information by integration of steps or optic-flow-based speed signals. In the insect brain, a region called the central complex plays a key role for path integration. Not only does the central complex house a ring-attractor network that encodes head directions, neurons responding to optic flow also converge with this circuit. A neural substrate for integrating direction and distance into a memorized home vector has therefore been proposed in the central complex. We discuss how behavioral data and the theoretical framework of path integration can be aligned with these neural data. Heinze, Narendra and Cheung discuss the fundamental principles of insect path integration behavior and highlight interactions with other navigational strategies using insights from behavioral data, the theoretical underpinnings, and from recent discoveries illuminating the neural control of path integration.
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| 5. |
- Immonen, Esa Ville, et al.
(författare)
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Anatomical organization of the brain of a diurnal and a nocturnal dung beetle
- 2017
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Ingår i: Journal of Comparative Neurology. - : Wiley. - 0021-9967. ; 525:8, s. 1879-1908
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Tidskriftsartikel (refereegranskat)abstract
- To avoid the fierce competition for food, South African ball-rolling dung beetles carve a piece of dung off a dung-pile, shape it into a ball and roll it away along a straight line path. For this unidirectional exit from the busy dung pile, at night and day, the beetles use a wide repertoire of celestial compass cues. This robust and relatively easily measurable orientation behavior has made ball-rolling dung beetles an attractive model organism for the study of the neuroethology behind insect orientation and sensory ecology. Although there is already some knowledge emerging concerning how celestial cues are processed in the dung beetle brain, little is known about its general neural layout. Mapping the neuropils of the dung beetle brain is thus a prerequisite to understand the neuronal network that underlies celestial compass orientation. Here, we describe and compare the brains of a day-active and a night-active dung beetle species based on immunostainings against synapsin and serotonin. We also provide 3D reconstructions for all brain areas and many of the fiber bundles in the brain of the day-active dung beetle. Comparison of neuropil structures between the two dung beetle species revealed differences that reflect adaptations to different light conditions. Altogether, our results provide a reference framework for future studies on the neuroethology of insects in general and dung beetles in particular.
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| 6. |
- Patel, Rickesh N., et al.
(författare)
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Parallel vector memories in the brain of a bee as foundation for flexible navigation
- 2024
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Ingår i: Proceedings of the National Academy of Sciences of the United States of America. - 1091-6490. ; 121:30, s. 2402509121-2402509121
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Tidskriftsartikel (refereegranskat)abstract
- Insects rely on path integration (vector-based navigation) and landmark guidance to perform sophisticated navigational feats, rivaling those seen in mammals. Bees in particular exhibit complex navigation behaviors including creating optimal routes and novel shortcuts between locations, an ability historically indicative of the presence of a cognitive map. A mammalian cognitive map has been widely accepted. However, in insects, the existence of a centralized cognitive map is highly contentious. Using a controlled laboratory assay that condenses foraging behaviors to short distances in walking bumblebees, we reveal that vectors learned during path integration can be transferred to long-term memory, that multiple such vectors can be stored in parallel, and that these vectors can be recalled at a familiar location and used for homeward navigation. These findings demonstrate that bees meet the two fundamental requirements of a vector-based analog of a decentralized cognitive map: Home vectors need to be stored in long-term memory and need to be recalled from remembered locations. Thus, our data demonstrate that bees possess the foundational elements for a vector-based map. By utilizing this relatively simple strategy for spatial organization, insects may achieve high-level navigation behaviors seen in vertebrates with the limited number of neurons in their brains, circumventing the computational requirements associated with the cognitive maps of mammals.
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| 7. |
- Stone, Thomas, et al.
(författare)
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An Anatomically Constrained Model for Path Integration in the Bee Brain
- 2017
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Ingår i: Current Biology. - : Elsevier BV. - 1879-0445 .- 0960-9822. ; 27:20, s. 11-3085
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Tidskriftsartikel (refereegranskat)abstract
- Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odometer-but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light-based compass neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy, we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically identified neurons suggested for each processing step. The resulting model circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e., a ground velocity that is not precisely aligned with body orientation) typical of bee flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings-suggesting a more basic function for central complex connectivity, from which path integration may have evolved.
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| 8. |
- Heinze, Stanley, et al.
(författare)
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A unified platform to manage, share, and archive morphological and functional data in insect neuroscience
- 2021
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Ingår i: eLife. - 2050-084X. ; 10
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Tidskriftsartikel (refereegranskat)abstract
- 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.
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| 9. |
- Adden, Andrea, et al.
(författare)
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A Neural Model for Insect Steering Applied to Olfaction and Path Integration
- 2022
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Ingår i: Neural Computation. - : MIT Press. - 0899-7667 .- 1530-888X. ; 34:11, s. 2205-2231
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Tidskriftsartikel (refereegranskat)abstract
- Many animal behaviors require orientation and steering with respect to the environment. For insects, a key brain area involved in spatial orientation and navigation is the central complex. Activity in this neural circuit has been shown to track the insect’s current heading relative to its environment and has also been proposed to be the substrate of path inte-gration. However, it remains unclear how the output of the central complex is integrated into motor commands. Central complex output neurons project to the lateral accessory lobes (LAL), from which descending neurons project to thoracic motor centers. Here, we present a computational model of a simple neural network that has been described anatomically and physiologically in the LALs of male silkworm moths, in the context of odor-mediated steering. We present and analyze two versions of this network, one rate based and one based on spiking neurons. The mod-eled network consists of an inhibitory local interneuron and a bistable descending neuron (flip-flop) that both receive input in the LAL. The flip-flop neuron projects onto neck motor neurons to induce steering. We show that this simple computational model not only replicates the basic parameters of male silkworm moth behavior in a simulated odor plume but can also take input from a computational model of path integration in the central complex and use it to steer back to a point of origin. Fur-thermore, we find that increasing the level of detail within the model im-proves the realism of the model’s behavior, leading to the emergence of looping behavior as an orientation strategy. Our results suggest that descending neurons originating in the LALs, such as flip-flop neurons, are sufficient to mediate multiple steering behaviors. This study is therefore a first step to close the gap between orientation circuits in the central complex and downstream motor centers.
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| 10. |
- Adden, Andrea, et al.
(författare)
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The brain of a nocturnal migratory insect, the Australian Bogong moth
- 2020
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Ingår i: Journal of Comparative Neurology. - : Wiley. - 0021-9967 .- 1096-9861. ; 528:11, s. 1942-1963
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Tidskriftsartikel (refereegranskat)abstract
- Every year, millions of Australian Bogong moths (Agrotis infusa) complete an astonishing journey: In Spring, they migrate over 1,000 km from their breeding grounds to the alpine regions of the Snowy Mountains, where they endure the hot summer in the cool climate of alpine caves. In autumn, the moths return to their breeding grounds, where they mate, lay eggs and die. These moths can use visual cues in combination with the geomagnetic field to guide their flight, but how these cues are processed and integrated into the brain to drive migratory behavior is unknown. To generate an access point for functional studies, we provide a detailed description of the Bogong moth's brain. Based on immunohistochemical stainings against synapsin and serotonin (5HT), we describe the overall layout as well as the fine structure of all major neuropils, including the regions that have previously been implicated in compass-based navigation. The resulting average brain atlas consists of 3D reconstructions of 25 separate neuropils, comprising the most detailed account of a moth brain to date. Our results show that the Bogong moth brain follows the typical lepidopteran ground pattern, with no major specializations that can be attributed to their spectacular migratory lifestyle. These findings suggest that migratory behavior does not require widespread modifications of brain structure, but might be achievable via small adjustments of neural circuitry in key brain areas. Locating these subtle changes will be a challenging task for the future, for which our study provides an essential anatomical framework.
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