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Natural variation in the courtship song of Drosophila is mapped to the intronic insertion of a retroelement at the slowpoke locus, which encodes an ion channel. On a wing and a song An important aspect of courtship behaviour in Drosophila is the male courtship song, generated when the males vibrate their wings. The features of this courtship song and how this varies between Drosophila species have been well-characterized. David Stern and colleagues now map the genetic variation causal for natural variation in courtship song between two wild isolates of D. simulans and D. mauritiana to the insertion of a retroelement at the slowpoke ( slo ) locus, which encodes an ion channel. Animal species display enormous variation for innate behaviours, but little is known about how this diversity arose. Here, using an unbiased genetic approach, we map a courtship song difference between wild isolates of Drosophila simulans and Drosophila mauritiana to a 966 base pair region within the slowpoke ( slo ) locus, which encodes a calcium-activated potassium channel 1 . Using the reciprocal hemizygosity test 2 , we confirm that slo is the causal locus and resolve the causal mutation to the evolutionarily recent insertion of a retroelement in a slo intron within D. simulans . Targeted deletion of this retroelement reverts the song phenotype and alters slo splicing. Like many ion channel genes, slo is expressed widely in the nervous system and influences a variety of behaviours 3 , 4 ; slo -null males sing little song with severely disrupted features. By contrast, the natural variant of slo alters a specific component of courtship song, illustrating that regulatory evolution of a highly pleiotropic ion channel gene can cause modular changes in behaviour.

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 . We show that behavioral ON-motion responses are more sensitive to UV than for OFF-motion, and we identify cellular pathways connecting UV-sensitive R7 photoreceptors to ON and OFF-motion-sensitive T4 and T5 cells, using neurogenetics and calcium imaging. Remarkably, this contribution of color circuitry to motion vision enhances the detection of approaching UV discs, but not green discs with the same chromatic contrast, and we show how this could generalize for systems with ON- and OFF-motion pathways. Our results provide a computational and circuit basis for how color enhances motion vision to favor the detection of saliently colored objects. Motion vision in many animals is split into pathways for bright (ON) and dark (OFF) edges, driven by luminance changes. Here the authors show how in Drosophila color selectively contributes to ON-motion, enhancing detection of saliently colored objects.

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.

The optokinetic nystagmus is a gaze-stabilizing mechanism reducing motion blur by rapid eye rotations against the direction of visual motion, followed by slower syndirectional eye movements minimizing retinal slip speed. Flies control their gaze through head turns controlled by neck motor neurons receiving input directly, or via descending neurons, from well-characterized directional-selective interneurons sensitive to visual wide-field motion. Locomotion increases the gain and speed sensitivity of these interneurons, while visual motion adaptation in walking animals has the opposite effects. To find out whether flies perform an optokinetic nystagmus, and how it may be affected by locomotion and visual motion adaptation, we recorded head movements of blowflies on a trackball stimulated by progressive and rotational visual motion. Flies flexibly responded to rotational stimuli with optokinetic nystagmus-like head movements, independent of their locomotor state. The temporal frequency tuning of these movements, though matching that of the upstream directional-selective interneurons, was only mildly modulated by walking speed or visual motion adaptation. Our results suggest flies flexibly control their gaze to compensate for rotational wide-field motion by a mechanism similar to an optokinetic nystagmus. Surprisingly, the mechanism is less state-dependent than the response properties of directional-selective interneurons providing input to the neck motor system.

Animal sensory systems are optimally adapted to those features typically encountered in natural surrounds, thus allowing neurons with limited bandwidth to encode challengingly large input ranges. Natural scenes are not random, and peripheral visual systems in vertebrates and insects have evolved to respond efficiently to their typical spatial statistics. The mammalian visual cortex is also tuned to natural spatial statistics, but less is known about coding in higher order neurons in insects. To redress this we here record intracellularly from a higher order visual neuron in the hoverfly. We show that the cSIFE neuron, which is inhibited by stationary images, is maximally inhibited when the slope constant of the amplitude spectrum is close to the mean in natural scenes. The behavioural optomotor response is also strongest to images with naturalistic image statistics. Our results thus reveal a close coupling between the inherent statistics of natural scenes and higher order visual processing in insects. Natural scenes contain statistics that are constrained in both space and time. Here, the authors show that, in insects as in mammals, both higher order neural mechanisms and behavioural discrimination are tuned to natural spatial statistics.

CA1 is the main source of efferents from the hippocampus, but the function of the cortical input to CA1 remains unclear. Normal CA1 place field activity is supported by this input after CA3 has been lesioned. However, inhibitory responses are observed in CA1 after the stimulation of the cortical input in slice preparations. An integrate-and-fire neuron model of the cortical-CA1 network is presented which accounts for both phenomena by using N-methyl- D-aspartate receptors to mediate a significant proportion of the excitatory response. The model demonstrates that a rate coding scheme is consistent with both phenomena, a remaining challenge to temporal coding schemes in the pathway.

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. Competing Interest Statement The authors have declared no competing interest.

Many animals use the visual motion generated by travelling straight, the translatory optic flow, to successfully navigate obstacles: near objects appear larger and to move more quickly than distant objects. Flies are expert at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. Here, we present novel cell types that have motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes forward sideslip self-motion, and fires action potentials in clusters - spike bursts. We show that the spike burst coding is size and speed-tuned, and is selectively modulated by motion parallax - the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the single spike rate is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have properties well-suited to the visual navigation of clutter and to encode movements along near cardinal axes of thrust, lift and forward sideslip.

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. To unravel the stunning diversity of a complex visual system, a careful mapping of the neural architecture matched to tools for targeted exploration of that circuitry is essential. Here, we report a new connectome of the right optic lobe from a male central nervous system FIB-SEM volume and a comprehensive inventory of the fly's visual neurons. We developed a computational framework to quantify the anatomy of visual neurons, establishing a basis for interpreting how their shapes relate to spatial vision. By integrating this analysis with connectivity information, neurotransmitter identity, and expert curation, we classified the ~53,000 neurons into 727 types, about half of which are systematically described and named for the first time. Finally, we share an extensive collection of split-GAL4 lines matched to our neuron type catalog. Together, this comprehensive set of tools and data unlock new possibilities for systematic investigations of vision in , a foundation for a deeper understanding of sensory processing.

Color and motion are used by many species to identify salient moving 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. We show that behavioral ON-motion responses are more sensitive to UV than for OFF-motion, and we identify cellular pathways connecting UV-sensitive R7 photoreceptors to ON and OFF-motion-sensitive T4 and T5 cells, using neurogenetics and calcium imaging. Remarkably, the synergy of color and motion vision enhances the detection of approaching UV discs, but not green discs with the same chromatic contrast, and we show how this generalizes for visual systems with ON and OFF pathways. Our results provide a computational and circuit basis for how color enhances motion vision to favor the detection of saliently colored objects.