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22 Janelia Publications

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    04/02/18 | Colour vision: A fresh view of lateral inhibition in Drosophila.
    Longden KD
    Current Biology : CB. 2018 Apr 02;28(7):R308-R311. doi: 10.1016/j.cub.2018.02.052

    A recent study reports a novel form of lateral inhibition between photoreceptors supporting colour vision in the vinegar fly, Drosophila melanogaster.

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    01/08/18 | Simple integration of fast excitation and offset, delayed inhibition computes directional selectivity in Drosophila.
    Gruntman E, Romani S, Reiser MB
    Nature Neuroscience. 2018 Jan 08;21(2):250-7. doi: 10.1038/s41593-017-0046-4

    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. Here we use in vivo whole-cell recordings of T4 to show that directional selectivity originates from simple integration of spatially offset fast excitatory and slow inhibitory inputs, resulting in a suppression of responses to the nonpreferred motion direction. We constructed a passive, conductance-based model of a T4 cell that accurately predicts the neuron's response to moving stimuli. These results connect the known circuit anatomy of the motion pathway to the algorithmic mechanism by which the direction of motion is computed.

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    Reiser LabRubin LabFly Functional Connectome
    12/18/17 | Behavioral state modulates the ON visual motion pathway of Drosophila.
    Strother JA, Wu S, Rogers EM, Eliason JL, Wong AM, Nern A, Reiser MB
    Proceedings of the National Academy of Sciences of the United States of America. 2017 Dec 18;115(1):E102-11. doi: 10.1073/pnas.1703090115

    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. Here, we show that the behavioral state alters the baseline activity levels and the temporal tuning of the first directionally selective neuron in the ON motion pathway (T4) as well as its primary input neurons (Mi1, Tm3, Mi4, Mi9). These effects are especially prominent in the inhibitory neuron Mi4, and we show that central octopaminergic neurons provide input to Mi4 and increase its excitability. We further show that octopamine neurons are required for sustained behavioral responses to fast-moving, but not slow-moving, visual stimuli in walking flies. These results indicate that behavioral-state modulation acts directly on the inputs to the directionally selective neurons and supports efficient neural coding of motion stimuli.

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    11/08/17 | Ultra-selective looming detection from radial motion opponency.
    Klapoetke NC, Nern A, Peek MY, Rogers EM, Breads P, Rubin GM, Reiser MB, Card GM
    Nature. 2017 Nov 08;551(7679):237-241. doi: 10.1038/nature24626

    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. Here we report the discovery of an ultra-selective looming detecting neuron, lobula plate/lobula columnar, type II (LPLC2) in Drosophila, and show how its selectivity is established by radial motion opponency. In the fly visual system, directionally selective small-field neurons called T4 and T5 form a spatial map in the lobula plate, where they each terminate in one of four retinotopic layers, such that each layer responds to motion in a different cardinal direction. Single-cell anatomical analysis reveals that each arm of the LPLC2 cross-shaped primary dendrites ramifies in one of these layers and extends along that layer's preferred motion direction. In vivo calcium imaging demonstrates that, as their shape predicts, individual LPLC2 neurons respond strongly to outward motion emanating from the centre of the neuron's receptive field. Each dendritic arm also receives local inhibitory inputs directionally selective for inward motion opposing the excitation. This radial motion opponency generates a balance of excitation and inhibition that makes LPLC2 non-responsive to related patterns of motion such as contraction, wide-field rotation or luminance change. As a population, LPLC2 neurons densely cover visual space and terminate onto the giant fibre descending neurons, which drive the jump muscle motor neuron to trigger an escape take off. Our findings provide a mechanistic description of the selective feature detection that flies use to discern and escape looming threats.

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    07/13/17 | Mapping the neural substrates of behavior.
    Robie AA, Hirokawa J, Edwards AW, Umayam LA, Lee A, Phillips ML, Card GM, Korff W, Rubin GM, Simpson JH, Reiser MB, Branson KM
    Cell. 2017-07-13;170(2):393-406. doi: 10.1016/j.cell.2017.06.032

    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. We combined a novel quantification of anatomy with our behavioral analysis to create brain-behavior correlation maps, which are shared as browsable web pages and interactive software. Based on these maps, we generated hypotheses of regions of the brain causally related to sensory processing, locomotor control, courtship, aggression, and sleep. Our maps directly specify genetic tools to target these regions, which we used to identify a small population of neurons with a role in the control of walking.

    •We developed machine-vision methods to broadly and precisely quantify fly behavior•We measured effects of activating 2,204 genetically targeted neuronal populations•We created whole-brain maps of neural substrates of locomotor and social behaviors•We created resources for exploring our results and enabling further investigation

    Machine-vision analyses of large behavior and neuroanatomy data reveal whole-brain maps of regions associated with numerous complex behaviors.

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    Rubin LabReiser LabFly Functional Connectome
    04/05/17 | The emergence of directional selectivity in the visual motion pathway of Drosophila.
    Strother JA, Wu S, Wong AM, Nern A, Rogers EM, Le JQ, Rubin GM, Reiser MB
    Neuron. 2017 Apr 05;94(1):168-182.e10. doi: 10.1016/j.neuron.2017.03.010

    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. Using calcium imaging, we found that these neuron types are not directionally selective and that selectivity arises in the T4 dendrites. By silencing each input neuron type, we identified which neurons are necessary for T4 directional selectivity and ON motion behavioral responses. We then determined the sign of the connections between these neurons and T4 cells using neuronal photoactivation. Our results indicate a computational architecture for motion detection that is a hybrid of classic theoretical models.

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    04/03/17 | Sensorimotor Neuroscience: Motor Precision Meets Vision.
    Longden KD, Huston SJ, Reiser MB
    Current Biology : CB. 2017 Apr 03;27(7):R261-R263. doi: 10.1016/j.cub.2017.02.047

    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.

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    01/13/17 | Electrophoresis of polar fluorescent tracers through the nerve sheath labels neuronal populations for anatomical and functional imaging.
    Isaacson MD, Hedwig B
    Scientific Reports. 2017 Jan 13;7:40433. doi: 10.1038/srep40433

    The delivery of tracers into populations of neurons is essential to visualize their anatomy and analyze their function. In some model systems genetically-targeted expression of fluorescent proteins is the method of choice; however, these genetic tools are not available for most organisms and alternative labeling methods are very limited. Here we describe a new method for neuronal labelling by electrophoretic dye delivery from a suction electrode directly through the neuronal sheath of nerves and ganglia in insects. Polar tracer molecules were delivered into the locust auditory nerve without destroying its function, simultaneously staining peripheral sensory structures and central axonal projections. Local neuron populations could be labelled directly through the surface of the brain, and in-vivo optical imaging of sound-evoked activity was achieved through the electrophoretic delivery of calcium indicators. The method provides a new tool for studying how stimuli are processed in peripheral and central sensory pathways and is a significant advance for the study of nervous systems in non-model organisms.

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    12/28/16 | Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs.
    Wu M, Nern A, Williamson WR, Morimoto MM, Reiser MB, Card GM, Rubin GM
    eLife. 2016 Dec 28;5:. doi: 10.7554/eLife.21022

    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 Drosophila 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. The activation phenotypes of two LC types closely resemble natural avoidance behaviors triggered by a visual loom. In vivo two-photon calcium imaging reveals that these LC types respond to looming stimuli, while another type does not, but instead responds to the motion of a small object. Activation of LC neurons on only one side of the brain can result in attractive or aversive turning behaviors depending on the cell type. Our results indicate that LC neurons convey information on the presence and location of visual features relevant for specific behaviors.

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    10/24/16 | Central brain circuitry for color-vision-modulated behaviors.
    Longden KD
    Current Biology : CB. 2016 Oct 24;26(20):R981-8. doi: 10.1016/j.cub.2016.07.071

    Color is famous for not existing in the external world: our brains create the perception of color from the spatial and temporal patterns of the wavelength and intensity of light. For an intangible quality, we have detailed knowledge of its origins and consequences. Much is known about the organization and evolution of the first phases of color processing, the filtering of light in the eye and processing in the retina, and about the final phases, the roles of color in behavior and natural selection. To understand how color processing in the central brain has evolved, we need well-defined pathways or circuitry where we can gauge how color contributes to the computations involved in specific behaviors. Examples of such pathways or circuitry that are dedicated to processing color cues are rare, despite the separation of color and luminance pathways early in the visual system of many species, and despite the traditional definition of color as being independent of luminance. This minireview presents examples in which color vision contributes to behaviors dominated by other visual modalities, examples that are not part of the canon of color vision circuitry. The pathways and circuitry process a range of chromatic properties of objects and their illumination, and are taken from a variety of species. By considering how color processing complements luminance processing, rather than being independent of it, we gain an additional way to account for the diversity of color coding in the central brain, its consequences for specific behaviors and ultimately the evolution of color vision.

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