Eye structure shapes neuron function in Drosophila motion vision.

Many animals use vision to navigate their environment. The pattern of changes that self-motion induces in the visual scene, referred to as optic flow, is first estimated in local patches by directionally selective neurons. However, how arrays of directionally selective neurons, each responsive to motion in a preferred direction at specific retinal positions, are organized to support robust decoding of optic flow by downstream circuits is unclear.

Whole-body physics simulation of fruit fly locomotion.

The body of an animal influences how its nervous system generates behaviour. Accurately modelling the neural control of sensorimotor behaviour requires an anatomically detailed biomechanical representation of the body. Here we introduce a whole-body model of the fruit fly Drosophila melanogaster in a physics simulator.

Connectome-driven neural inventory of a complete visual system.

Vision provides animals with detailed information about their surroundings and conveys diverse features such as colour, form and movement across the visual scene. Computing these parallel spatial features requires a large and diverse network of neurons. Consequently, from flies to humans, visual regions in the brain constitute half its volume.

Connectome-driven neural inventory of a complete visual system.

Vision provides animals with detailed information about their surroundings, conveying diverse features such as color, form, and movement across the visual scene. Computing these parallel spatial features requires a large and diverse network of neurons, such that in animals as distant as flies and humans, visual regions comprise half the brain's volume. These visual brain regions often reveal remarkable structure-function relationships, with neurons organized along spatial maps with shapes that directly relate to their roles in visual processing.

Homeodomain proteins hierarchically specify neuronal diversity and synaptic connectivity.

How our brain generates diverse neuron types that assemble into precise neural circuits remains unclear. Using lamina neuron types (L1-L5), we show that the primary homeodomain transcription factor (HDTF) brain-specific homeobox (Bsh) is initiated in progenitors and maintained in L4/L5 neurons to adulthood. Bsh activates secondary HDTFs Ap (L4) and Pdm3 (L5) and specifies L4/L5 neuronal fates while repressing the HDTF Zfh1 to prevent ectopic L1/L3 fates (control: L1-L5; Bsh-knockdown: L1-L3), thereby generating lamina neuronal diversity for normal visual sensitivity.

Different spectral sensitivities of ON- and OFF-motion pathways enhance the detection of approaching color objects in Drosophila.

Color and motion are used by many species to identify salient objects. They are processed largely independently, but color contributes to motion processing in humans, for example, enabling moving colored objects to be detected when their luminance matches the background. Here, we demonstrate an unexpected, additional contribution of color to motion vision in Drosophila.

A comprehensive neuroanatomical survey of the Lobula Plate Tangential Neurons with predictions for their optic flow sensitivity.

Flying insects exhibit remarkable navigational abilities controlled by their compact nervous systems. , the pattern of changes in the visual scene induced by locomotion, is a crucial sensory cue for robust self-motion estimation, especially during rapid flight. Neurons that respond to specific, large-field optic flow patterns have been studied for decades, primarily in large flies, such as houseflies, blowflies, and hover flies.

Neuronal circuits integrating visual motion information in Drosophila melanogaster.

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.

A functionally ordered visual feature map in the Drosophila brain.

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.

Synaptic targets of photoreceptors specialized to detect color and skylight polarization in .

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 , and we have used light microscopy to confirm many of our findings.

Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion.

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.

An Inexpensive, High-Precision, Modular Spherical Treadmill Setup Optimized for Experiments.

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.

Spatial readout of visual looming in the central brain of .

Visual systems can exploit spatial correlations in the visual scene by using retinotopy, the organizing principle by which neighboring cells encode neighboring spatial locations. 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.

A genetic, genomic, and computational resource for exploring neural circuit function.

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.

The computation of directional selectivity in the OFF motion pathway.

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.

Simple integration of fast excitation and offset, delayed inhibition computes directional selectivity in Drosophila.

A neuron that extracts directionally selective motion information from upstream signals lacking this selectivity must compare visual responses from spatially offset inputs. Distinguishing among prevailing algorithmic models for this computation requires measuring fast neuronal activity and inhibition. In the Drosophila melanogaster visual system, a fourth-order neuron-T4-is the first cell type in the ON pathway to exhibit directionally selective signals.

Behavioral state modulates the ON visual motion pathway of .

The behavioral state of an animal can dynamically modulate visual processing. In flies, the behavioral state is known to alter the temporal tuning of neurons that carry visual motion information into the central brain. However, where this modulation occurs and how it tunes the properties of this neural circuit are not well understood.

Ultra-selective looming detection from radial motion opponency.

Nervous systems combine lower-level sensory signals to detect higher-order stimulus features critical to survival, such as the visual looming motion created by an imminent collision or approaching predator. Looming-sensitive neurons have been identified in diverse animal species. Different large-scale visual features such as looming often share local cues, which means loom-detecting neurons face the challenge of rejecting confounding stimuli.

Mapping the Neural Substrates of Behavior.

Assigning behavioral functions to neural structures has long been a central goal in neuroscience and is a necessary first step toward a circuit-level understanding of how the brain generates behavior. Here, we map the neural substrates of locomotion and social behaviors for Drosophila melanogaster using automated machine-vision and machine-learning techniques. From videos of 400,000 flies, we quantified the behavioral effects of activating 2,204 genetically targeted populations of neurons.

The Emergence of Directional Selectivity in the Visual Motion Pathway of Drosophila.

The perception of visual motion is critical for animal navigation, and flies are a prominent model system for exploring this neural computation. In Drosophila, the T4 cells of the medulla are directionally selective and necessary for ON motion behavioral responses. To examine the emergence of directional selectivity, we developed genetic driver lines for the neuron types with the most synapses onto T4 cells.

Sensorimotor Neuroscience: Motor Precision Meets Vision.

Visual motion sensing neurons in the fly also encode a range of behavior-related signals. These nonvisual inputs appear to be used to correct some of the challenges of visually guided locomotion.

Visual projection neurons in the lobula link feature detection to distinct behavioral programs.

Visual projection neurons (VPNs) provide an anatomical connection between early visual processing and higher brain regions. Here we characterize lobula columnar (LC) cells, a class of VPNs that project to distinct central brain structures called optic glomeruli. We anatomically describe 22 different LC types and show that, for several types, optogenetic activation in freely moving flies evokes specific behaviors.

Wide-field feedback neurons dynamically tune early visual processing.

An important strategy for efficient neural coding is to match the range of cellular responses to the distribution of relevant input signals. However, the structure and relevance of sensory signals depend on behavioral state. Here, we show that behavior modifies neural activity at the earliest stages of fly vision.

Direct observation of ON and OFF pathways in the Drosophila visual system.

Visual motion perception is critical to many animal behaviors, and flies have emerged as a powerful model system for exploring this fundamental neural computation. Although numerous studies have suggested that fly motion vision is governed by a simple neural circuit [1-3], the implementation of this circuit has remained mysterious for decades. Connectomics and neurogenetics have produced a surge in recent progress, and several studies have shown selectivity for light increments (ON) or decrements (OFF) in key elements associated with this circuit [4-7].