Biology subjects

Wernet, M. F.

Publications and source records attributed to Wernet, M. F..

9 recordsLinked to original sources

bioRxiv2023

Connectomic reconstruction predicts the functional organization of visual inputs to the navigation center of the Drosophila brain

Many animals, including humans, navigate their surroundings by visual input, yet we understand little about how visual information is transformed and integrated by the navigation system. In Drosophila melanogaster, compass neurons in the donut-shaped ellipsoid body of the central complex generate a sense of direction by integrating visual input from ring neurons, a part of the anterior visual pathway (AVP). Here, we densely reconstruct all neurons in the AVP using FlyWire, an AI-assisted tool for analyzing electron-microscopy data. The AVP comprises four neuropils, sequentially linked by three major classes of neurons: MeTu neurons, which connect the medulla in the optic lobe to the small unit of anterior optic tubercle (AOTUsu) in the central brain; TuBu neurons, which connect the anterior optic tubercle to the bulb neuropil; and ring neurons, which connect the bulb to the ellipsoid body. Based on neuronal morphologies, connectivity between different neural classes, and the locations of synapses, we identified non-overlapping channels originating from four types of MeTu neurons, which we further divided into ten subtypes based on the presynaptic connections in medulla and postsynaptic connections in AOTUsu. To gain an objective measure of the natural variation within the pathway, we quantified the differences between anterior visual pathways from both hemispheres and between two electron-microscopy datasets. Furthermore, we infer potential visual features and the visual area from which any given ring neuron receives input by combining the connectivity of the entire AVP, the MeTu neurons dendritic fields, and presynaptic connectivity in the optic lobes. These results provide a strong foundation for understanding how distinct visual features are extracted and transformed across multiple processing stages to provide critical information for computing the flys sense of direction.

neuroscience↗

bioRxiv2023

Individuality across environmental context in Drosophila melanogaster

Over the past decade, several studies have demonstrated that idiosyncratic animal behaviors remain consistent over long time periods. The consistency of individually variable behaviors over time is often referred to as an animals individuality, or if consisting of multiple traits personality. However, most experimental studies have focused on individuality in a single, well-defined environmental context, whereas it is well-established from population studies that animal behavior is highly context-dependent. The person-situation debate in humans and decades of observations of animal individuality under intrinsically variable natural conditions raise the question of whether and to what extent animal behavior remains consistent across different situations, such as changing environmental contexts. For instance, one individual might be generally more visually guided than another, or rely only on one particular visual cue, or even on this very cue only in a specific environmental context. Here, we use a combination of both well-established and novel behavioral assays to demonstrate the relationship between individual behavior and variable environmental context under tightly controlled laboratory conditions in the model system Drosophila melanogaster. The consistency of three individual traits (termed exploration, attention, and anxiety) was investigated under changing environmental contexts (temperature, visual cues, arena shape), in both walking and flying flies. We find that individuality is highly context-dependent, but even under the most extreme environmental alterations tested, consistency of behavioral individuality always persisted in at least one of the traits. Furthermore, our quantification reveals a hierarchical order of environmental features influencing individuality. We confirmed this hierarchy using a generalized linear model and a hierarchical linear mixed model. In summary, our work demonstrates that, similar to humans, fly individuality persists across different contexts (albeit worse than across time), and individual differences shape behavior across variable environments. The presence of consistency across situations in flies makes the underlying developmental and functional mechanisms amenable to genetic dissection.

animal behavior and cognition↗

bioRxiv2022

Behavioral responses of free flying Drosophila melanogaster to shiny, reflecting surfaces

Active locomotion plays an important role in the life of many animals since it permits to explore the environment and find vital resources. Most insect species rely on a combination of visual cues such as celestial bodies, landmarks, or linearly polarized light to navigate or to orient themselves in their surroundings. In nature, linearly polarized light can arise either from atmospheric scattering or from reflections off shiny non-metallic surfaces like water or shiny foil. Although multiple reports described different behavioral responses of various insects to such shiny surfaces, little is known about the retinal detectors or the underlying neural circuits. Our goal was to quantify the behavioral responses of free flying Drosophila melanogaster, a molecular genetic model organism that allows for systematic dissection of neural circuitry. Fruit flies were placed in a custom-built arena with controlled environmental parameters (temperature, humidity, and light intensity). Flight densities and landings were quantified for hydrated and dehydrated fly populations when separately exposed to three different stimuli such as a diffusely-reflecting matt plate, a small patch of shiny foil, versus real water. Our analysis reveals for the first time that flying fruit flies indeed use vision to guide their flight maneuvers around shiny surfaces.

animal behavior and cognition↗

bioRxiv2021

Synaptic targets of functionally specialized R7 and R8 photoreceptors in the central eye and dorsal rim area of Drosophila

Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

neuroscience↗

bioRxiv2020

Parallel visual pathways with topographic versus non-topographic organization connect the Drosophila eyes to the central brain

One hallmark of the visual system is the strict retinotopic organization from the periphery towards the central brain, spanning multiple layers of synaptic integration. Recent Drosophila studies on the computation of distinct visual features have shown that retinotopic representation is often lost beyond the optic lobes, due to convergence of columnar neuron types onto optic glomeruli. Nevertheless, functional imaging revealed a spatially accurate representation of visual cues in the central complex (CX), raising the question how this is implemented on a circuit level. By characterizing the afferents to a specific visual glomerulus, the anterior optic tubercle (AOTU), we discovered a spatial segregation of topographic versus non-topographic projections from molecularly distinct classes of medulla projection neurons (medullo-tubercular, or MeTu neurons). Distinct classes of topographic versus non-topographic MeTus form parallel channels, terminating in separate AOTU domains. Both types then synapse onto separate matching topographic fields of tubercular-bulbar (TuBu) neurons which relay visual information towards the dendritic fields of central complex ring neurons in the bulb neuropil, where distinct bulb sectors correspond to a distinct ring domain in the ellipsoid body. Hence, peripheral topography is maintained due to stereotypic circuitry within each TuBu class, providing the structural basis for spatial representation of visual information in the central complex. Together with previous data showing rough topography of lobula projections to a different AOTU subunit, our results further highlight the AOTUs role as a prominent relay station for spatial information from the retina to the central brain.

neuroscience↗

bioRxiv2019

Cellular and synaptic adaptations of neural circuits processing skylight polarization in the fly

Specialized ommatidia harboring polarization-sensitive photoreceptors exist in the dorsal rim area (DRA) of virtually all insects. Although downstream elements have been described both anatomically and physiologically throughout the optic lobes and the central brain of different species, little is known about their cellular and synaptic adaptations and how these shape their functional role in polarization vision. We have previously shown that in the DRA of Drosophila melanogaster, two distinct types of modality-specific distal medulla cell types (Dm-DRA1 and Dm-DRA2) are post-synaptic to long visual fiber photoreceptors R7 and R8, respectively. Here we describe additional neuronal elements in the medulla neuropil that manifest modality-specific differences in the DRA region, including DRA-specific neuronal morphology, as well as differences in the structure of pre- or post-synaptic membranes. Furthermore, we show that certain cell types (medulla tangential cells and octopaminergic neuromodulatory cells) specifically avoid contacts with polarization-sensitive photoreceptors. Finally, while certain transmedullary cells are specifically absent from DRA medulla columns, other subtypes show specific wiring differences while still connecting the DRA to the lobula complex, as previously been described in larger insects. This hints towards a complex circuit architecture with more than one pathway connecting polarization-sensitive DRA photoreceptors with the central brain.

neuroscience↗

bioRxiv2019

Heading choices of flying Drosophila under changing angles of polarized light

Many navigating insects include the celestial polarization pattern as an additional visual cue to orient their travels. Spontaneous orientation responses of both walking and flying fruit flies (Drosophila melanogaster) to linearly polarized light have previously been demonstrated. Using newly designed modular flight arenas consisting entirely of off-the-shelf parts and 3D-printed components we present individual flying flies with a slow and continuous rotational change in the incident angle of linear polarization. Under such open-loop conditions, single flies choose arbitrary headings with respect to the angle of polarized light and show a clear tendency to maintain those chosen headings for several minutes, thereby adjusting their course to the slow rotation of the incident stimulus. Importantly, flies show the tendency to maintain a chosen heading even when two individual test periods under a linearly polarized stimulus are interrupted by an epoch of unpolarized light lasting several minutes. Finally, we show that these behavioral responses are wavelength-specific, existing under polarized UV stimulus while being absent under polarized green light. Taken together, these findings provide further evidence supporting Drosophilas abilities to use celestial cues for visually guided navigation and course correction.

neuroscience↗

bioRxiv2019

Modality-specific circuits for skylight orientation in the fly visual system

In the fly optic lobe [~]800 highly stereotypical columnar microcircuits are arranged retinotopically to process visual information. Differences in cellular composition and synaptic connectivity within functionally specialized columns remains largely unknown. Here we describe the cellular and synaptic architecture in medulla columns located downstream of photoreceptors in the dorsal rim area (DRA), where linearly polarized skylight is detected for guiding orientation responses. We show that only in DRA medulla columns, both R7 and R8 photoreceptors target to the bona fide R7 target layer where they form connections with previously uncharacterized, modality-specific Dm neurons: Two morphologically distinct DRA-specific cell types (termed Dm-DRA1 and Dm-DRA2) stratify in separate sublayers and exclusively contact polarization-sensitive DRA inputs, while avoiding overlaps with color-sensitive Dm8 cells. Using the activity-dependent GRASP and trans-Tango techniques, we confirm that DRA R7 cells are synaptically connected to Dm-DRA1, whereas DRA R8 form synapses with Dm-DRA2. Finally, using live imaging of ingrowing pupal photoreceptor axons, we show that DRA R7 and R8 termini reach layer M6 sequentially, thus separating the establishment of different synaptic connectivity in time. We propose that a duplication of R7[->]Dm circuitry in DRA ommatidia serves as an ideal adaptation for detecting linearly polarized skylight using orthogonal e-vector analyzers.

neuroscience↗

bioRxiv2019

New modular assays for the quantitative study of skylight navigation in flying flies

The quantitative study of visual behaviors using virtual flight arenas is complicated by the fact that an effective experimental setup needs to combine a rather complex set of custom-built mechanical, electronic, and software components. Assembling such an apparatus amounts to a major challenge when working in an environment without the support of a machine shop. Here we present detailed instructions for the assembly of virtual flight arenas optimized for Drosophila skylight navigation, which can easily be modified towards other uses. This system consists entirely of off-the-shelf parts and 3D-printed components, combining a modular flight arena designed to reduce visual artifacts, swappable high-power LED light sources, polarization filters on a computer-controlled rotating filter wheel, all placed within a temperature and humidity controlled environment. Using this new assay, we show that individual flies choose arbitrary headings when flying under a uniform field of linear polarization. Furthermore, flies adjust their heading to both sudden and continuous changes in filter orientation and can keep their chosen heading for several minutes. Finally, flies show the tendency to maintain headings even after interruption with an unpolarized stimulus. Taken together, these findings demonstrate the usefulness of these assays for the study of skylight navigation in flies.

neuroscience↗