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51 Publications

Showing 11-20 of 51 results
03/10/23 | Drosophila antennae are dispensable for gravity orientation
Nikolay Kladt , Michael B. Reiser
bioRxiv. 2023 Mar 10:. doi: 10.1101/2023.03.08.531317

The nearly constant downward force of gravity has powerfully shaped the behaviors of many organisms [1]. Walking flies readily orient against gravity in a behavior termed negative gravitaxis. In Drosophila this behavior is studied by observing the position of flies in vials [24] or simple mazes [59]. These assays have been used to conduct forward-genetic screens [568] and as simple tests of locomotion deficits [1012]. Despite this long history of investigation, the sensory basis of gravitaxis is largely unknown [1]. Recent studies have implicated the antennae as a major mechanosensory input [34], but many details remain unclear. Fly orientation behavior is expected to depend on the direction and amplitude of the gravitational pull, but little is known about the sensitivity of flies to these features of the environment. Here we directly measure the gravity-dependent orientation behavior of flies walking on an adjustable tilted platform, that is inspired by previous insect studies [1316]. In this arena, flies can freely orient with respect to gravity. Our findings indicate that flies are exquisitely sensitive to the direction of gravity’s pull. Surprisingly, this orientation behavior does not require antennal mechanosensory input, suggesting that other sensory structures must be involved.

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12/15/22 | Eye structure shapes neuron function in Drosophila motion vision
Arthur Zhao , Eyal Gruntman , Aljoscha Nern , Nirmala A. Iyer , Edward M. Rogers , Sanna Koskela , Igor Siwanowicz , Marisa Dreher , Miriam A. Flynn , Connor W. Laughland , Henrique D.F. Ludwig , Alex G. Thomson , Cullen P. Moran , Bruck Gezahegn , Davi D. Bock , Michael B. Reiser
bioRxiv. 2022 Dec 15:. doi: 10.1101/2022.12.14.520178

Many animals rely on vision to navigate through their environment. The pattern of changes in the visual scene induced by self-motion is the optic flow1, which is first estimated in local patches by directionally selective (DS) neurons24. But how should the arrays of DS neurons, each responsive to motion in a preferred direction at a specific retinal position, be organized to support robust decoding of optic flow by downstream circuits? Understanding this global organization is challenging because it requires mapping fine, local features of neurons across the animal’s field of view3. In Drosophila, the asymmetric dendrites of the T4 and T5 DS neurons establish their preferred direction, making it possible to predict DS responses from anatomy4,5. Here we report that the preferred directions of fly DS neurons vary at different retinal positions and show that this spatial variation is established by the anatomy of the compound eye. To estimate the preferred directions across the visual field, we reconstructed hundreds of T4 neurons in a full brain EM volume6 and discovered unexpectedly stereotypical dendritic arborizations that are independent of location. We then used whole-head μCT scans to map the viewing directions of all compound eye facets and found a non-uniform sampling of visual space that explains the spatial variation in preferred directions. Our findings show that the organization of preferred directions in the fly is largely determined by the compound eye, exposing an intimate and unexpected connection between the peripheral structure of the eye, functional properties of neurons deep in the brain, and the control of body movements.

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08/22/22 | Neuronal circuits integrating visual motion information in Drosophila melanogaster.
Shinomiya K, Nern A, Meinertzhagen IA, Plaza SM, Reiser MB
Current Biology. 2022 Aug 22;32(16):3529-3544. doi: 10.1016/j.cub.2022.06.061

The detection of visual motion enables sophisticated animal navigation, and studies on flies have provided profound insights into the cellular and circuit bases of this neural computation. The fly's directionally selective T4 and T5 neurons encode ON and OFF motion, respectively. Their axons terminate in one of the four retinotopic layers in the lobula plate, where each layer encodes one of the four directions of motion. Although the input circuitry of the directionally selective neurons has been studied in detail, the synaptic connectivity of circuits integrating T4/T5 motion signals is largely unknown. Here, we report a 3D electron microscopy reconstruction, wherein we comprehensively identified T4/T5's synaptic partners in the lobula plate, revealing a diverse set of new cell types and attributing new connectivity patterns to the known cell types. Our reconstruction explains how the ON- and OFF-motion pathways converge. T4 and T5 cells that project to the same layer connect to common synaptic partners and comprise a core motif together with bilayer interneurons, detailing the circuit basis for computing motion opponency. We discovered pathways that likely encode new directions of motion by integrating vertical and horizontal motion signals from upstream T4/T5 neurons. Finally, we identify substantial projections into the lobula, extending the known motion pathways and suggesting that directionally selective signals shape feature detection there. The circuits we describe enrich the anatomical basis for experimental and computations analyses of motion vision and bring us closer to understanding complete sensory-motor pathways.

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05/18/22 | A functionally ordered visual feature map in the Drosophila brain.
Klapoetke NC, Nern A, Rogers EM, Rubin GM, Reiser MB, Card GM
Neuron. 2022 May 18;110(10):1700. doi: 10.1016/j.neuron.2022.02.013

Topographic maps, the systematic spatial ordering of neurons by response tuning, are common across species. In Drosophila, the lobula columnar (LC) neuron types project from the optic lobe to the central brain, where each forms a glomerulus in a distinct position. However, the advantages of this glomerular arrangement are unclear. Here, we examine the functional and spatial relationships of 10 glomeruli using single-neuron calcium imaging. We discover novel detectors for objects smaller than the lens resolution (LC18) and for complex line motion (LC25). We find that glomeruli are spatially clustered by selectivity for looming versus drifting object motion and ordered by size tuning to form a topographic visual feature map. Furthermore, connectome analysis shows that downstream neurons integrate from sparse subsets of possible glomeruli combinations, which are biased for glomeruli encoding similar features. LC neurons are thus an explicit example of distinct feature detectors topographically organized to facilitate downstream circuit integration.

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12/16/21 | Synaptic targets of photoreceptors specialized to detect color and skylight polarization in .
Kind E, Longden KD, Nern A, Zhao A, Sancer G, Flynn MA, Laughland CW, Gezahegn B, Ludwig HD, Thomson AG, Obrusnik T, Alarcón PG, Dionne H, Bock DD, Rubin GM, Reiser MB, Wernet MF
eLife. 2021 Dec 16;10:. doi: 10.7554/eLife.71858

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.

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12/06/21 | Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion.
Gruntman E, Reimers P, Romani S, Reiser MB
Current Biology. 2021 Dec 06;31(23):5286. doi: 10.1016/j.cub.2021.09.072

Diverse sensory systems, from audition to thermosensation, feature a separation of inputs into ON (increments) and OFF (decrements) signals. In the Drosophila visual system, separate ON and OFF pathways compute the direction of motion, yet anatomical and functional studies have identified some crosstalk between these channels. We used this well-studied circuit to ask whether the motion computation depends on ON-OFF pathway crosstalk. Using whole-cell electrophysiology, we recorded visual responses of T4 (ON) and T5 (OFF) cells, mapped their composite ON-OFF receptive fields, and found that they share a similar spatiotemporal structure. We fit a biophysical model to these receptive fields that accurately predicts directionally selective T4 and T5 responses to both ON and OFF moving stimuli. This model also provides a detailed mechanistic explanation for the directional preference inversion in response to the prominent reverse-phi illusion. Finally, we used the steering responses of tethered flying flies to validate the model's predicted effects of varying stimulus parameters on the behavioral turning inversion.

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07/16/21 | An inexpensive, high-precision, modular spherical treadmill setup optimized for experiments.
Loesche F, Reiser MB
Frontiers in Behavioral Neuroscience. 2021 Jul 16;15:689573. doi: 10.3389/fnbeh.2021.689573

To pursue a more mechanistic understanding of the neural control of behavior, many neuroethologists study animal behavior in controlled laboratory environments. One popular approach is to measure the movements of restrained animals while presenting controlled sensory stimulation. This approach is especially powerful when applied to genetic model organisms, such as , where modern genetic tools enable unprecedented access to the nervous system for activity monitoring or targeted manipulation. While there is a long history of measuring the behavior of body- and head-fixed insects walking on an air-supported ball, the methods typically require complex setups with many custom components. Here we present a compact, simplified setup for these experiments that achieves high-performance at low cost. The simplified setup integrates existing hardware and software solutions with new component designs. We replaced expensive optomechanical and custom machined components with off-the-shelf and 3D-printed parts, and built the system around a low-cost camera that achieves 180 Hz imaging and an inexpensive tablet computer to present view-angle-corrected stimuli updated through a local network. We quantify the performance of the integrated system and characterize the visually guided behavior of flies in response to a range of visual stimuli. In this paper, we thoroughly document the improved system; the accompanying repository incorporates CAD files, parts lists, source code, and detailed instructions. We detail a complete ~$300 system, including a cold-anesthesia tethering stage, that is ideal for hands-on teaching laboratories. This represents a nearly 50-fold cost reduction as compared to a typical system used in research laboratories, yet is fully featured and yields excellent performance. We report the current state of this system, which started with a 1-day teaching lab for which we built seven parallel setups and continues toward a setup in our lab for larger-scale analysis of visual-motor behavior in flies. Because of the simplicity, compactness, and low cost of this system, we believe that high-performance measurements of tethered insect behavior should now be widely accessible and suitable for integration into many systems. This access enables broad opportunities for comparative work across labs, species, and behavioral paradigms.

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11/18/20 | Spatial readout of visual looming in the central brain of Drosophila.
Morimoto MM, Nern A, Zhao A, Rogers EM, Wong A, Isaacson MD, Bock D, Rubin GM, Reiser MB
eLife. 2020 Nov 18;9:. doi: 10.7554/eLife.57685

Visual systems can exploit spatial correlations in the visual scene by using retinotopy. However, retinotopy is often lost, such as when visual pathways are integrated with other sensory modalities. How is spatial information processed outside of strictly visual brain areas? Here, we focused on visual looming responsive LC6 cells in , a population whose dendrites collectively cover the visual field, but whose axons form a single glomerulus-a structure without obvious retinotopic organization-in the central brain. We identified multiple cell types downstream of LC6 in the glomerulus and found that they more strongly respond to looming in different portions of the visual field, unexpectedly preserving spatial information. Through EM reconstruction of all LC6 synaptic inputs to the glomerulus, we found that LC6 and downstream cell types form circuits within the glomerulus that enable spatial readout of visual features and contralateral suppression-mechanisms that transform visual information for behavioral control.

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01/15/20 | A genetic, genomic, and computational resource for exploring neural circuit function.
Davis FP, Nern A, Picard S, Reiser MB, Rubin GM, Eddy SR, Henry GL
eLife. 2020 Jan 15;9:. doi: 10.7554/eLife.50901

The anatomy of many neural circuits is being characterized with increasing resolution, but their molecular properties remain mostly unknown. Here, we characterize gene expression patterns in distinct neural cell types of the visual system using genetic lines to access individual cell types, the TAPIN-seq method to measure their transcriptomes, and a probabilistic method to interpret these measurements. We used these tools to build a resource of high-resolution transcriptomes for 100 driver lines covering 67 cell types, available at http://www.opticlobe.com. Combining these transcriptomes with recently reported connectomes helps characterize how information is transmitted and processed across a range of scales, from individual synapses to circuit pathways. We describe examples that include identifying neurotransmitters, including cases of apparent co-release, generating functional hypotheses based on receptor expression, as well as identifying strong commonalities between different cell types.

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12/11/19 | The computation of directional selectivity in the OFF motion pathway.
Gruntman E, Romani S, Reiser MB
eLife. 2019 Dec 11;8:. doi: 10.7554/eLife.50706

In flies, the direction of moving ON and OFF features is computed separately. T4 (ON) and T5 (OFF) are the first neurons in their respective pathways to extract a directionally selective response from their non-selective inputs. Our recent study of T4 found that the integration of offset depolarizing and hyperpolarizing inputs is critical for the generation of directional selectivity. However, T5s lack small-field inhibitory inputs, suggesting they may use a different mechanism. Here we used whole-cell recordings of T5 neurons and found a similar receptive field structure: fast depolarization and persistent, spatially offset hyperpolarization. By assaying pairwise interactions of local stimulation across the receptive field, we found no amplifying responses, only suppressive responses to the non-preferred motion direction. We then evaluated passive, biophysical models and found that a model using direct inhibition, but not the removal of excitation, can accurately predict T5 responses to a range of moving stimuli.

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