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82 Publications

Showing 1-10 of 82 results
03/27/20 | Unc-4 acts to promote neuronal identity and development of the take-off circuit in the Drosophila CNS.
Lacin H, Williamson WR, Card GM, Skeath JB, Truman JW
eLife. 2020 Mar 27;9:. doi: 10.7554/eLife.55007
03/23/20 | Recurrent architecture for adaptive regulation of learning in the insect brain.
Eschbach C, Fushiki A, Winding M, Schneider-Mizell CM, Shao M, Arruda R, Eichler K, Valdes-Aleman J, Ohyama T, Thum AS, Gerber B, Fetter RD, Truman JW, Litwin-Kumar A, Cardona A, Zlatic M, Cardona A, Zlatic M
Nature Neuroscience. 2020 Mar 23;23(4):544-55. doi: 10.1038/s41593-020-0607-9

Dopaminergic neurons (DANs) drive learning across the animal kingdom, but the upstream circuits that regulate their activity and thereby learning remain poorly understood. We provide a synaptic-resolution connectome of the circuitry upstream of all DANs in a learning center, the mushroom body of Drosophila larva. We discover afferent sensory pathways and a large population of neurons that provide feedback from mushroom body output neurons and link distinct memory systems (aversive and appetitive). We combine this with functional studies of DANs and their presynaptic partners and with comprehensive circuit modeling. We find that DANs compare convergent feedback from aversive and appetitive systems, which enables the computation of integrated predictions that may improve future learning. Computational modeling reveals that the discovered feedback motifs increase model flexibility and performance on learning tasks. Our study provides the most detailed view to date of biological circuit motifs that support associative learning.

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10/15/19 | Developmental organization of central neurons in the adult Drosophila ventral nervous system.
Shepherd D, Sahota V, Court R, Williams DW, Truman JW
Journal of Comparative Neurology. 2019 Oct 15;527(15):2573-2598. doi: 10.1002/cne.24690

We have used MARCM to reveal the adult morphology of the post embryonically produced neurons in the thoracic neuromeres of the Drosophila VNS. The work builds on previous studies of the origins of the adult VNS neurons to describe the clonal organization of the adult VNS. We present data for 58 of 66 postembryonic thoracic lineages, excluding the motor neuron producing lineages (15 and 24) which have been described elsewhere. MARCM labels entire lineages but where both A and B hemilineages survive (e.g., lineages 19, 12, 13, 6, 1, 3, 8, and 11), the two hemilineages can be discriminated and we have described each hemilineage separately. Hemilineage morphology is described in relation to the known functional domains of the VNS neuropil and based on the anatomy we are able to assign broad functional roles for each hemilineage. The data show that in a thoracic hemineuromere, 16 hemilineages are primarily involved in controlling leg movements and walking, 9 are involved in the control of wing movements, and 10 interface between both leg and wing control. The data provide a baseline of understanding of the functional organization of the adult Drosophila VNS. By understanding the morphological organization of these neurons, we can begin to define and test the rules by which neuronal circuits are assembled during development and understand the functional logic and evolution of neuronal networks.

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Truman LabCardona Lab
06/14/19 | Regulation of forward and backward locomotion through intersegmental feedback circuits in Drosophila larvae.
Kohsaka H, Zwart MF, Fushiki A, Fetter RD, Truman JW, Cardona A, Nose A
Nature Communications. 2019 Jun 14;10(1):2654. doi: 10.1038/s41467-019-10695-y

Animal locomotion requires spatiotemporally coordinated contraction of muscles throughout the body. Here, we investigate how contractions of antagonistic groups of muscles are intersegmentally coordinated during bidirectional crawling of Drosophila larvae. We identify two pairs of higher-order premotor excitatory interneurons present in each abdominal neuromere that intersegmentally provide feedback to the adjacent neuromere during motor propagation. The two feedback neuron pairs are differentially active during either forward or backward locomotion but commonly target a group of premotor interneurons that together provide excitatory inputs to transverse muscles and inhibitory inputs to the antagonistic longitudinal muscles. Inhibition of either feedback neuron pair compromises contraction of transverse muscles in a direction-specific manner. Our results suggest that the intersegmental feedback neurons coordinate contraction of synergistic muscles by acting as delay circuits representing the phase lag between segments. The identified circuit architecture also shows how bidirectional motor networks could be economically embedded in the nervous system.

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03/26/19 | Neurotransmitter identity is acquired in a lineage-restricted manner in the Drosophila CNS.
Lacin H, Chen H, Long X, Singer RH, Lee T, Truman JW
Elife. 2019 Mar 26;8:. doi: 10.7554/eLife.43701

The vast majority of the adult fly ventral nerve cord is composed of 34 hemilineages, which are clusters of lineally related neurons. Neurons in these hemilineages use one of the three fast-acting neurotransmitters (acetylcholine, GABA, or glutamate) for communication. We generated a comprehensive neurotransmitter usage map for the entire ventral nerve cord. We did not find any cases of neurons using more than one neurotransmitter, but found that the acetylcholine specific gene ChAT is transcribed in many glutamatergic and GABAergic neurons, but these transcripts typically do not leave the nucleus and are not translated. Importantly, our work uncovered a simple rule: All neurons within a hemilineage use the same neurotransmitter. Thus, neurotransmitter identity is acquired at the stem cell level. Our detailed transmitter- usage/lineage identity map will be a great resource for studying the developmental basis of behavior and deciphering how neuronal circuits function to regulate behavior.

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Cardona LabTruman LabZlatic Lab
01/29/19 | Neural substrates of Drosophila larval anemotaxis.
Jovanic T, Winding M, Cardona A, Truman JW, Gershow M, Zlatic M
Current Biology : CB. 2019 Jan 29;29(4):554-66. doi: 10.1016/j.cub.2019.01.009

Animals use sensory information to move toward more favorable conditions. Drosophila larvae can move up or down gradients of odors (chemotax), light (phototax), and temperature (thermotax) by modulating the probability, direction, and size of turns based on sensory input. Whether larvae can anemotax in gradients of mechanosensory cues is unknown. Further, although many of the sensory neurons that mediate taxis have been described, the central circuits are not well understood. Here, we used high-throughput, quantitative behavioral assays to demonstrate Drosophila larvae anemotax in gradients of wind speeds and to characterize the behavioral strategies involved. We found that larvae modulate the probability, direction, and size of turns to move away from higher wind speeds. This suggests that similar central decision-making mechanisms underlie taxis in somatosensory and other sensory modalities. By silencing the activity of single or very few neuron types in a behavioral screen, we found two sensory (chordotonal and multidendritic class III) and six nerve cord neuron types involved in anemotaxis. We reconstructed the identified neurons in an electron microscopy volume that spans the entire larval nervous system and found they received direct input from the mechanosensory neurons or from each other. In this way, we identified local interneurons and first- and second-order subesophageal zone (SEZ) and brain projection neurons. Finally, silencing a dopaminergic brain neuron type impairs anemotaxis. These findings suggest that anemotaxis involves both nerve cord and brain circuits. The candidate neurons and circuitry identified in our study provide a basis for future detailed mechanistic understanding of the circuit principles of anemotaxis.

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Fetter LabTruman LabCardona Lab
12/11/18 | Convergence of monosynaptic and polysynaptic sensory paths onto common motor outputs in a feeding connectome.
Miroschnikow A, Schlegel P, Schoofs A, Hueckesfeld S, Li F, Schneider-Mizell CM, Fetter RD, Truman JW, Cardona A, Pankratz MJ
eLife. 2018 Dec 11;7:. doi: 10.7554/eLife.40247

We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior of larvae. Input neurons originate from enteric, pharyngeal and external sensory organs and converge onto seven distinct sensory synaptic compartments within the CNS. Output neurons consist of feeding motor, serotonergic modulatory and neuroendocrine neurons. Monosynaptic connections from a set of sensory synaptic compartments cover the motor, modulatory and neuroendocrine targets in overlapping domains. Polysynaptic routes are superimposed on top of monosynaptic connections, resulting in divergent sensory paths that converge on common outputs. A completely different set of sensory compartments is connected to the mushroom body calyx. The mushroom body output neurons are connected to interneurons that directly target the feeding output neurons. Our results illustrate a circuit architecture in which monosynaptic and multisynaptic connections from sensory inputs traverse onto output neurons via a series of converging paths.

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Truman LabZlatic LabCardona Lab
11/22/18 | Sensorimotor pathway controlling stopping behavior during chemotaxis in the larva.
Tastekin I, Khandelwal A, Tadres D, Fessner ND, Truman JW, Zlatic M, Cardona A, Louis M
eLife. 2018 Nov 22;7:. doi: 10.7554/eLife.38740

Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the larva, the detection of positive odor gradients extends runs while negative gradients promote stops and turns. This algorithm represents a foundation for the control of sensory navigation across phyla. In the present work, we identified an olfactory descending neuron, PDM-DN, which plays a pivotal role in the organization of stops and turns in response to the detection of graded changes in odor concentrations. Artificial activation of this descending neuron induces deterministic stops followed by the initiation of turning maneuvers through head casts. Using electron microscopy, we reconstructed the main pathway that connects the PDM-DN neuron to the peripheral olfactory system and to the pre-motor circuit responsible for the actuation of forward peristalsis. Our results set the stage for a detailed mechanistic analysis of the sensorimotor conversion of graded olfactory inputs into action selection to perform goal-oriented navigation.

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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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Zlatic LabTruman Lab
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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