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18 Janelia Publications

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    Jumping in planthopper and froghopper insects is propelled by a catapult-like mechanism requiring mechanical storage of energy and its quick release to accelerate the hind legs rapidly. To understand the functional biomechanics involved in these challenging movements, the internal skeleton, tendons and muscles involved were reconstructed in 3-D from confocal scans in unprecedented detail. Energy to power jumping was generated by slow contractions of hind leg depressor muscles and then stored by bending specialised elements of the thoracic skeleton that are composites of the rubbery protein resilin sandwiched between layers of harder cuticle with air-filled tunnels reducing mass. The images showed that the lever arm of the power-producing muscle changed in magnitude during jumping, but at all joint angles would cause depression, suggesting a mechanism by which the stored energy is released. This methodological approach illuminates how miniaturized components interact and function in complex and rapid movements of small animals.

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    Gonen Lab
    06/20/17 | MicroED structures from micrometer thick protein crystals.
    Martynowycz M, Glynn C, Miao J, de la Cruz MJ, Hattne J, Shi D, Cascio D, Rodriguez J, Gonen T
    bioRxiv. 2017 Jun 20:. doi: 10.1101/152504

    Theoretical calculations suggest that crystals exceeding 100 nm thickness are excluded by dynamical scattering from successful structure determination using microcrystal electron diffraction (MicroED). These calculations are at odds with experimental results where MicroED structures have been determined from significantly thicker crystals. Here we systematically evaluate the influence of thickness on the accuracy of MicroED intensities and the ability to determine structures from protein crystals one micrometer thick. To do so, we compare ab initio structures of a human prion protein segment determined from thin crystals to those determined from crystals up to one micrometer thick. We also compare molecular replacement solutions from crystals of varying thickness for a larger globular protein, proteinase K. Our results indicate that structures can be reliably determined from crystals at least an order of magnitude thicker than previously suggested by simulation, opening the possibility for an even broader range of MicroED experiments.

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    06/12/17 | Neural signatures of dynamic stimulus selection in Drosophila.
    Sun Y, Nern A, Franconville R, Dana H, Schreiter ER, Looger LL, Svoboda K, Kim DS, Hermundstad AM, Jayaraman V
    Nature Neuroscience. 2017 Jun 12;20(8):1104-13. doi: 10.1038/nn.4581

    Many animals orient using visual cues, but how a single cue is selected from among many is poorly understood. Here we show that Drosophila ring neurons—central brain neurons implicated in navigation—display visual stimulus selection. Using in vivo two-color two-photon imaging with genetically encoded calcium indicators, we demonstrate that individual ring neurons inherit simple-cell-like receptive fields from their upstream partners. Stimuli in the contralateral visual field suppressed responses to ipsilateral stimuli in both populations. Suppression strength depended on when and where the contralateral stimulus was presented, an effect stronger in ring neurons than in their upstream inputs. This history-dependent effect on the temporal structure of visual responses, which was well modeled by a simple biphasic filter, may determine how visual references are selected for the fly's internal compass. Our approach highlights how two-color calcium imaging can help identify and localize the origins of sensory transformations across synaptically connected neural populations.

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    06/07/17 | A protocol demonstrating 60 different Drosophila behaviors in one assay.
    McKellar CE, Wyttenbach RA
    Journal of Undergraduate Neuroscience Education (JUNE). 2017 Spring;15(2):A110-6

    The fruit fly Drosophila melanogaster performs many behaviors, from simple motor actions to complex social interactions, that are of interest to neurobiologists studying how the brain controls behavior. Here, an undergraduate laboratory exercise uses cutting-edge methods to activate sets of neurons thermogenetically, triggering 60 different behaviors. Students learn how to recognize this large repertoire of behaviors from 16 fly strains that are publicly available, and from a large set of training videos provided here. A full protocol, timeline and handouts are included. Instructors need not have any experience working with flies. Student feedback is reported; in our experience, students are fascinated and highly engaged by watching animals perform such a broad array of behaviors. This exercise teaches fly husbandry and crossing, careful scientific observation, and principles of behavioral screening.

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    Svoboda Lab
    06/07/17 | Mechanisms underlying a thalamocortical transformation during active tactile sensation.
    Gutnisky DA, Yu J, Hires SA, To M, Bale M, Svoboda K, Golomb D
    PLoS Computational Biology. 2017 Jun 07;13(6):e1005576. doi: 10.1371/journal.pcbi.1005576

    During active somatosensation, neural signals expected from movement of the sensors are suppressed in the cortex, whereas information related to touch is enhanced. This tactile suppression underlies low-noise encoding of relevant tactile features and the brain's ability to make fine tactile discriminations. Layer (L) 4 excitatory neurons in the barrel cortex, the major target of the somatosensory thalamus (VPM), respond to touch, but have low spike rates and low sensitivity to the movement of whiskers. Most neurons in VPM respond to touch and also show an increase in spike rate with whisker movement. Therefore, signals related to self-movement are suppressed in L4. Fast-spiking (FS) interneurons in L4 show similar dynamics to VPM neurons. Stimulation of halorhodopsin in FS interneurons causes a reduction in FS neuron activity and an increase in L4 excitatory neuron activity. This decrease of activity of L4 FS neurons contradicts the "paradoxical effect" predicted in networks stabilized by inhibition and in strongly-coupled networks. To explain these observations, we constructed a model of the L4 circuit, with connectivity constrained by in vitro measurements. The model explores the various synaptic conductance strengths for which L4 FS neurons actively suppress baseline and movement-related activity in layer 4 excitatory neurons. Feedforward inhibition, in concert with recurrent intracortical circuitry, produces tactile suppression. Synaptic delays in feedforward inhibition allow transmission of temporally brief volleys of activity associated with touch. Our model provides a mechanistic explanation of a behavior-related computation implemented by the thalamocortical circuit.

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    06/07/17 | Memory retrieval from first principles.
    Katkov M, Romani S, Tsodyks M
    Neuron. 2017 Jun 07;94(5):1027-1032. doi: 10.1016/j.neuron.2017.03.048

    The dilemma that neurotheorists face is that (1) detailed biophysical models that can be constrained by direct measurements, while being of great importance, offer no immediate insights into cognitive processes in the brain, and (2) high-level abstract cognitive models, on the other hand, while relevant for understanding behavior, are largely detached from neuronal processes and typically have many free, experimentally unconstrained parameters that have to be tuned to a particular data set and, hence, cannot be readily generalized to other experimental paradigms. In this contribution, we propose a set of "first principles" for neurally inspired cognitive modeling of memory retrieval that has no biologically unconstrained parameters and can be analyzed mathematically both at neuronal and cognitive levels. We apply this framework to the classical cognitive paradigm of free recall. We show that the resulting model accounts well for puzzling behavioral data on human participants and makes predictions that could potentially be tested with neurophysiological recording techniques.

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    06/05/17 | Drosophila courtship conditioning as a measure of learning and memory.
    Koemans TS, Oppitz C, Donders RA, van Bokhoven H, Schenck A, Keleman K, Kramer JM
    Journal of Visualized Experiments - Neuroscience . 2017-06-05(124):e55808. doi: 10.3791/55808

    Many insights into the molecular mechanisms underlying learning and memory have been elucidated through the use of simple behavioral assays in model organisms such as the fruit fly, Drosophila melanogasterDrosophila is useful for understanding the basic neurobiology underlying cognitive deficits resulting from mutations in genes associated with human cognitive disorders, such as intellectual disability (ID) and autism. This work describes a methodology for testing learning and memory using a classic paradigm in Drosophilaknown as courtship conditioning. Male flies court females using a distinct pattern of easily recognizable behaviors. Premated females are not receptive to mating and will reject the male's copulation attempts. In response to this rejection, male flies reduce their courtship behavior. This learned reduction in courtship behavior is measured over time, serving as an indicator of learning and memory. The basic numerical output of this assay is the courtship index (CI), which is defined as the percentage of time that a male spends courting during a 10 min interval. The learning index (LI) is the relative reduction of CI in flies that have been exposed to a premated female compared to naïve flies with no previous social encounters. For the statistical comparison of LIs between genotypes, a randomization test with bootstrapping is used. To illustrate how the assay can be used to address the role of a gene relating to learning and memory, the pan-neuronal knockdown of Dihydroxyacetone phosphate acyltransferase (Dhap-at) was characterized here. The human ortholog of Dhap-atglyceronephosphate O-acyltransferase (GNPT), is involved in rhizomelic chondrodysplasia punctata type 2, an autosomal-recessive syndrome characterized by severe ID. Using the courtship conditioning assay, it was determined that Dhap-at is required for long-term memory, but not for short-term memory. This result serves as a basis for further investigation of the underlying molecular mechanisms.

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    Harris LabSinger LabTranscription ImagingFly Functional Connectome
    06/05/17 | Quantitative mRNA imaging throughout the entire Drosophila brain.
    Long X, Colonell J, Wong AM, Singer RH, Lionnet T
    Nature Methods. 2017 Jun 05;14(7):703-6. doi: 10.1038/nmeth.4309

    We describe a fluorescence in situ hybridization method that permits detection of the localization and abundance of single mRNAs (smFISH) in cleared whole-mount adult Drosophila brains. The approach is rapid and multiplexable and does not require molecular amplification; it allows facile quantification of mRNA expression with subcellular resolution on a standard confocal microscope. We further demonstrate single-mRNA detection across the entire brain using a custom Bessel beam structured illumination microscope (BB-SIM).

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