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44 Janelia Publications

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    Riddiford LabTruman LabRubin Lab
    04/04/18 | Juvenile hormone reveals mosaic developmental programs in the metamorphosing optic lobe of Drosophila melanogaster.
    Riddiford LM, Truman JW, Nern A
    Biology Open. 2018 Apr 04:. doi: 10.1242/bio.034025

    The development of the adult optic lobe (OL) of is directed by a wave of ingrowth of the photoreceptors over a two day period at the outset of metamorphosis which is accompanied by the appearance of the pupal-specific transcription factor Broad-Z3 (Br-Z3) and expression of early drivers in OL neurons. During this time, there are pulses of ecdysteroids that time the metamorphic events. At the outset, the transient appearance of juvenile hormone (JH) prevents precocious development of the OL caused by the ecdysteroid peak that initiates pupariation, but the artificial maintenance of JH after this time misdirects subsequent development. Axon ingrowth, Br-Z3 appearance and the expression of early drivers were unaffected, but aspects of later development such as the dendritic expansion of the lamina monopolar neurons and the expression of late drivers were suppressed. This effect of the exogenous JH mimic (JHM) pyriproxifen is lost by 24 hr after pupariation. Part of this effect of JHM is due to its suppression of the appearance of ecdysone receptor EcR-B1 that occurs after pupation and during early adult development.

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    03/28/18 | Dedicated photoreceptor pathways in Drosophila larvae mediate navigation by processing either spatial or temporal cues.
    Humberg T, Bruegger P, Afonso B, Zlatic M, Truman JW, Gershow M, Samuel A, Sprecher SG
    Nature Communications. 2018 Mar 28;9(1):1260. doi: 10.1038/s41467-018-03520-5

    To integrate changing environmental cues with high spatial and temporal resolution is critical for animals to orient themselves. Drosophila larvae show an effective motor program to navigate away from light sources. How the larval visual circuit processes light stimuli to control navigational decision remains unknown. The larval visual system is composed of two sensory input channels, Rhodopsin5 (Rh5) and Rhodopsin6 (Rh6) expressing photoreceptors (PRs). We here characterize how spatial and temporal information are used to control navigation. Rh6-PRs are required to perceive temporal changes of light intensity during head casts, while Rh5-PRs are required to control behaviors that allow navigation in response to spatial cues. We characterize how distinct behaviors are modulated and identify parallel acting and converging features of the visual circuit. Functional features of the larval visual circuit highlight the principle of how early in a sensory circuit distinct behaviors may be computed by partly overlapping sensory pathways.

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    03/16/18 | Functional architecture of reward learning in mushroom body extrinsic neurons of larval Drosophila.
    Saumweber T, Rohwedder A, Schleyer M, Eichler K, Chen Y, Aso Y, Cardona A, Eschbach C, Kobler O, Voigt A, Durairaja A, Mancini N, Zlatic M, Truman JW, Thum AS, Gerber B
    Nature Communications. 2018 Mar 16;9(1):1104. doi: 10.1038/s41467-018-03130-1

    The brain adaptively integrates present sensory input, past experience, and options for future action. The insect mushroom body exemplifies how a central brain structure brings about such integration. Here we use a combination of systematic single-cell labeling, connectomics, transgenic silencing, and activation experiments to study the mushroom body at single-cell resolution, focusing on the behavioral architecture of its input and output neurons (MBINs and MBONs), and of the mushroom body intrinsic APL neuron. Our results reveal the identity and morphology of almost all of these 44 neurons in stage 3 Drosophila larvae. Upon an initial screen, functional analyses focusing on the mushroom body medial lobe uncover sparse and specific functions of its dopaminergic MBINs, its MBONs, and of the GABAergic APL neuron across three behavioral tasks, namely odor preference, taste preference, and associative learning between odor and taste. Our results thus provide a cellular-resolution study case of how brains organize behavior.

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    01/16/18 | Repetitive aggressive encounters generate a long-lasting internal state in Drosophila melanogaster males.
    Kim Y, Saver M, Simon J, Kent CF, Shao L, Eddison M, Agrawal P, Texada M, Truman JW, Heberlein U
    Proceedings of the National Academy of Sciences of the United States of America. 2018 Jan 16;115(5):1099-104. doi: 10.1073/pnas.1716612115

    Multiple studies have investigated the mechanisms of aggressive behavior in Drosophila; however, little is known about the effects of chronic fighting experience. Here, we investigated if repeated fighting encounters would induce an internal state that could affect the expression of subsequent behavior. We trained wild-type males to become winners or losers by repeatedly pairing them with hypoaggressive or hyperaggressive opponents, respectively. As described previously, we observed that chronic losers tend to lose subsequent fights, while chronic winners tend to win them. Olfactory conditioning experiments showed that winning is perceived as rewarding, while losing is perceived as aversive. Moreover, the effect of chronic fighting experience generalized to other behaviors, such as gap-crossing and courtship. We propose that in response to repeatedly winning or losing aggressive encounters, male flies form an internal state that displays persistence and generalization; fight outcomes can also have positive or negative valence. Furthermore, we show that the activities of the PPL1-γ1pedc dopaminergic neuron and the MBON-γ1pedc>α/β mushroom body output neuron are required for aversion to an olfactory cue associated with losing fights.

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    01/08/18 | Neural substrates of navigational decision-making in Drosophila larva anemotaxis.
    Jovanic T, Truman JW, Gershow M, Zlatic M
    bioRxiv. 2018 Jan 08:244608. doi: 10.1101/244608

    Small animals navigate in the environment as a function of varying sensory information in order to reach more favorable environmental conditions. To achieve this Drosophila larvae alternate periods of runs and turns in gradients of light, temperature, odors and CO2. While the sensory neurons that mediate the navigation behaviors in the different sensory gradients have been described, where and how are these navigational strategies are implemented in the central nervous system and controlled by neuronal circuit elements is not well known. Here we characterize for the first time the navigational strategies of Drosophila larvae in gradients of air-current speeds using high-throughput behavioral assays and quantitative behavioral analysis. We find that larvae extend runs when facing favorable conditions and increase turn rate when facing unfavorable direction, a strategy they use in other sensory modalities as well. By silencing the activity of individual neurons and very sparse expression patterns (2 or 3 neuron types), we further identify the sensory neurons and circuit elements in the ventral nerve cord and brain of the larva required for navigational decisions during anemotaxis. The phenotypes of these central neurons are consistent with a mechanism where the increase of the turning rate in unfavorable conditions and decrease in turning rate in favorable conditions are independently controlled.

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    12/20/17 | Divergent connectivity of homologous command-like neurons mediates segment-specific touch responses in Drosophila.
    Takagi S, Cocanougher BT, Niki S, Miyamoto D, Kohsaka H, Kazama H, Fetter RD, Truman JW, Zlatic M, Cardona A, Nose A
    Neuron. 2017 Dec 20;96(6):1373-87. doi: 10.1016/j.neuron.2017.10.030

    Animals adaptively respond to a tactile stimulus by choosing an ethologically relevant behavior depending on the location of the stimuli. Here, we investigate how somatosensory inputs on different body segments are linked to distinct motor outputs in Drosophila larvae. Larvae escape by backward locomotion when touched on the head, while they crawl forward when touched on the tail. We identify a class of segmentally repeated second-order somatosensory interneurons, that we named Wave, whose activation in anterior and posterior segments elicit backward and forward locomotion, respectively. Anterior and posterior Wave neurons extend their dendrites in opposite directions to receive somatosensory inputs from the head and tail, respectively. Downstream of anterior Wave neurons, we identify premotor circuits including the neuron A03a5, which together with Wave, is necessary for the backward locomotion touch response. Thus, Wave neurons match their receptive field to appropriate motor programs by participating in different circuits in different segments.

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    11/10/17 | larvalign: Aligning gene expression patterns from the larval brain of Drosophila melanogaster.
    Muenzing SE, Strauch M, Truman JW, Bühler K, Thum AS, Merhof D
    Neuroinformatics. 2017 Nov 10:. doi: 10.1007/s12021-017-9349-6

    The larval brain of the fruit fly Drosophila melanogaster is a small, tractable model system for neuroscience. Genes for fluorescent marker proteins can be expressed in defined, spatially restricted neuron populations. Here, we introduce the methods for 1) generating a standard template of the larval central nervous system (CNS), 2) spatial mapping of expression patterns from different larvae into a reference space defined by the standard template. We provide a manually annotated gold standard that serves for evaluation of the registration framework involved in template generation and mapping. A method for registration quality assessment enables the automatic detection of registration errors, and a semi-automatic registration method allows one to correct registrations, which is a prerequisite for a high-quality, curated database of expression patterns. All computational methods are available within the larvalign software package: https://github.com/larvalign/larvalign/releases/tag/v1.0.

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    08/09/17 | The complete connectome of a learning and memory centre in an insect brain.
    Eichler K, Li F, Litwin-Kumar A, Park Y, Andrade I, Schneider-Mizell CM, Saumweber T, Huser A, Eschbach C, Gerber B, Fetter RD, Truman JW, Priebe CE, Abbott LF, Thum AS, Zlatic M, Cardona A
    Nature. 2017 Aug 09;548(7666):175-182. doi: 10.1038/nature23455

    Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higher-order circuit supporting associative memory has not been previously available. Here we reconstruct one such circuit at synaptic resolution, the Drosophila larval mushroom body. We find that most Kenyon cells integrate random combinations of inputs but that a subset receives stereotyped inputs from single projection neurons. This organization maximizes performance of a model output neuron on a stimulus discrimination task. We also report a novel canonical circuit in each mushroom body compartment with previously unidentified connections: reciprocal Kenyon cell to modulatory neuron connections, modulatory neuron to output neuron connections, and a surprisingly high number of recurrent connections between Kenyon cells. Stereotyped connections found between output neurons could enhance the selection of learned behaviours. The complete circuit map of the mushroom body should guide future functional studies of this learning and memory centre.

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    08/08/17 | Organization of the drosophila larval visual circuit.
    Larderet I, Fritsch PM, Gendre N, Neagu-Maier GL, Fetter RD, Schneider-Mizell CM, Truman JW, Zlatic M, Cardona A, Sprecher SG
    eLife. 2017 Aug 8:e28387. doi: 10.7554/eLife.28387

    Visual systems transduce, process and transmit light-dependent environmental cues. Computation of visual features depends on photoreceptor neuron types (PR) present, organization of the eye and wiring of the underlying neural circuit. Here, we describe the circuit architecture of the visual system of Drosophila larvae by mapping the synaptic wiring diagram and neurotransmitters. By contacting different targets, the two larval PR-subtypes create two converging pathways potentially underlying the computation of ambient light intensity and temporal light changes already within this first visual processing center. Locally processed visual information then signals via dedicated projection interneurons to higher brain areas including the lateral horn and mushroom body. The stratified structure of the larval optic neuropil (LON) suggests common organizational principles with the adult fly and vertebrate visual systems. The complete synaptic wiring diagram of the LON paves the way to understanding how circuits with reduced numerical complexity control wide ranges of behaviors.

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    07/01/17 | The Ol1mpiad: concordance of behavioural faculties of stage 1 and stage 3 Drosophila larvae.
    Almeida-Carvalho MJ, Berh D, Braun A, Chen Y, Eichler K, Eschbach C, Fritsch PM, Gerber B, Hoyer N, Jiang X, Kleber J, Klämbt C, König C, Louis M, Michels B, Miroschnikow A, Mirth C, Miura D, Niewalda T, Otto N, Paisios E, Pankratz MJ, Petersen M, Ramsperger N, Randel N, Risse B, Saumweber T, Schlegel P, Schleyer M, Soba P, Sprecher SG, Tanimura T, Thum AS, Toshima N, Truman JW, Yarali A, Zlatic M
    The Journal of Experimental Biology. 2017 Jul 01;220(Pt 13):2452-2475. doi: 10.1242/jeb.156646

    Mapping brain function to brain structure is a fundamental task for neuroscience. For such an endeavour, the Drosophila larva is simple enough to be tractable, yet complex enough to be interesting. It features about 10,000 neurons and is capable of various taxes, kineses and Pavlovian conditioning. All its neurons are currently being mapped into a light-microscopical atlas, and Gal4 strains are being generated to experimentally access neurons one at a time. In addition, an electron microscopic reconstruction of its nervous system seems within reach. Notably, this electron microscope-based connectome is being drafted for a stage 1 larva - because stage 1 larvae are much smaller than stage 3 larvae. However, most behaviour analyses have been performed for stage 3 larvae because their larger size makes them easier to handle and observe. It is therefore warranted to either redo the electron microscopic reconstruction for a stage 3 larva or to survey the behavioural faculties of stage 1 larvae. We provide the latter. In a community-based approach we called the Ol1mpiad, we probed stage 1 Drosophila larvae for free locomotion, feeding, responsiveness to substrate vibration, gentle and nociceptive touch, burrowing, olfactory preference and thermotaxis, light avoidance, gustatory choice of various tastants plus odour-taste associative learning, as well as light/dark-electric shock associative learning. Quantitatively, stage 1 larvae show lower scores in most tasks, arguably because of their smaller size and lower speed. Qualitatively, however, stage 1 larvae perform strikingly similar to stage 3 larvae in almost all cases. These results bolster confidence in mapping brain structure and behaviour across developmental stages.

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