James W. Truman's research while affiliated with Howard Hughes Medical Institute and other places

Publications (364)

Article
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We have focused on the mushroom bodies (MB) of Drosophila to determine how the larval circuits are formed and then transformed into those of the adult at metamorphosis. The adult MB has a core of thousands of Kenyon neurons; axons of the early-born g class form a medial lobe and those from later-born a'b' and ab classes form both medial and vertica...
Article
During postembryonic life, hormones, including ecdysteroids, juvenile hormones, insulin-like peptides, and activin/TGFβ ligands act to transform the larval nervous system into an adult version, which is a fine-grained mosaic of recycled larval neurons and adult-specific neurons. Hormones provide both instructional signals that make cells competent...
Preprint
Insects like Drosophila produce a second brain adapted to the form and behavior of a larva. Neurons for both larval and adult brains are produced by the same stem cells (neuroblasts) but the larva possesses only the earliest born neurons produced from each. To understand how a functional larval brain is made from this reduced set of neurons, we exa...
Article
Significance The genome of insects with complete metamorphosis contains the instructions for making three distinct body forms, that of the larva, of the pupa, and of the adult. However, the molecular mechanisms by which each gene set is called forth and stably expressed are poorly understood. A half century ago, it was proposed that there was a set...
Article
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Animal behavior is shaped both by evolution and by individual experience. Parallel brain pathways encode innate and learned valences of cues, but the way in which they are integrated during action-selection is not well understood. We used electron microscopy to comprehensively map with synaptic resolution all neurons downstream of all Mushroom Body...
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Neuroendocrine systems in animals maintain organismal homeostasis and regulate stress response. Although a great deal of work has been done on the neuropeptides and hormones that are released and act on target organs in the periphery, the synaptic inputs onto these neuroendocrine outputs in the brain are less well understood. Here, we use the trans...
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The mechanisms specifying neuronal diversity are well-characterized, yet it remains unclear how or if these mechanisms regulate neural circuit assembly. To address this, we mapped the developmental origin of 160 interneurons from seven bilateral neural progenitors (neuroblasts), and identify them in a synapse-scale TEM reconstruction of the Drosoph...
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Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural ci...
Preprint
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biorxiv link (article and supplements): https://www.biorxiv.org/content/10.1101/2020.10.22.350306v1.article-info Neuroendocrine systems in animals maintain organismal homeostasis and regulate stress response. Although a great deal of work has been done on the neuropeptides and hormones that are released and act on target organs in the periphery,...
Article
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Drosophila melanogaster is an established model for neuroscience research with relevance in biology and medicine. Until recently, research on the Drosophila brain was hindered by the lack of a complete and uniform nomenclature. Recognizing this, Ito et al. (2014) • Ito K. • Shinomiya K. • Ito M. • Armstrong D.J. • Boyan G. • Hartenstein V. • Harzs...
Article
Drosophila melanogaster is an established model for neuroscience research with relevance in biology and medicine. Until recently, research on the Drosophila brain was hindered by the lack of a complete and uniform nomenclature. Recognizing this, Ito et al. (2014) produced an authoritative nomenclature for the adult insect brain, using Drosophila as...
Preprint
Full-text available
Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural ci...
Preprint
Animal behavior is shaped both by evolution and by individual experience. In many species parallel brain pathways are thought to encode innate and learnt behavior drives and as a result may link the same sensory cue to different actions if innate and learnt drives are in opposition. How these opposing drives are integrated into a single coherent ac...
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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 pathwa...
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The Drosophila ventral nerve cord (VNC) is composed of thousands of neurons born from a set of individually identifiable stem cells. The VNC harbors neuronal circuits required to execute key behaviors, such as flying and walking. Leveraging the lineage-based functional organization of the VNC, we investigated the developmental and molecular basis o...
Article
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The Drosophila ventral nerve cord (VNC) is composed of thousands of neurons born from a set of individually identifiable stem cells. The VNC harbors neuronal circuits required to execute key behaviors, such as flying and walking. Leveraging the lineage-based functional organization of the VNC, we investigated the developmental and molecular basis o...
Article
Full-text available
The Drosophila ventral nerve cord (VNC) is composed of thousands of neurons born from a set of individually identifiable stem cells. The VNC harbors neuronal circuits required to execute key behaviors, such as flying and walking. Leveraging the lineage-based functional organization of the VNC, we investigated the developmental and molecular basis o...
Preprint
Full-text available
The Drosophila ventral nerve cord (VNC), the fly equivalent of the spinal cord, is composed of thousands of neurons that are born from a set of individually identifiable stem cells. The VNC harbors neuronal circuits required for the execution of vital behaviors, such as flying and walking. Taking advantage of the lineage-based functional organizati...
Article
The evolution of insect metamorphosis is one of the most important sagas in animal history, transforming small, obscure soil arthropods into a dominant terrestrial group that has profoundly shaped the evolution of terrestrial life. The evolution of flight initiated the trajectory towards metamorphosis, favoring enhanced differences between juvenile...
Article
Developmental, genetic and endocrine data from diverse taxa provide insight into the evolution of insect metamorphosis. We equate the larva–pupa–adult of the Holometabola to the pronymph–nymph–adult of hemimetabolous insects. The hemimetabolous pronymph is a cryptic embryonic stage with unique endocrinology and behavioural modifications that probab...
Preprint
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Molecular profiles of neurons influence information processing, but bridging the gap between genes, circuits and behavior has been very difficult. Furthermore, the behavioral state of an animal continuously changes across development and as a result of sensory experience. How behavioral state influences molecular cell state is poorly understood. He...
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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 abdomi...
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Modulatory ( e.g. dopaminergic) neurons provide 'teaching signals' that drive associative learning across the animal kingdom, but the circuit mechanisms by which these signals are computed are still unclear. To provide a basis for understanding the circuit implementation of learning algorithms, we generated a synaptic-resolution connectivity map of...
Preprint
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The mechanisms specifying neuronal diversity are well-characterized, yet it remains unclear how these mechanisms are used to establish neuronal morphology and connectivity. Here we map the developmental origin of over 78 neurons from seven identified neural progenitors (neuroblasts) within a complete TEM reconstruction of the Drosophila larval CNS....
Article
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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 (Harris et al., 2015; Shepherd et al., 2016; Truman et al., 2004) to describe the clonal organization of the adult VNS. We present...
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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 n...
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We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior of Drosophila 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, serot...
Article
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We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior of Drosophila 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, serot...
Article
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Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the Drosophila melanogaster 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 th...
Preprint
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Little is known about the organization of central circuits by which external and internal sensory in-puts act on motor outputs to regulate fundamental behaviors such as feeding. We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food in-take behavior of Drosophila larvae. The input neurons origi...
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The development of the adult optic lobe (OL) ofDrosophila melanogasteris 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 a...
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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 co...
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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 bo...
Preprint
Small animals use sensory information to navigate their environment in order to reach more favorable conditions. in gradients of light, temperature, odors and CO 2 , Drosophila larvae alternate periods of runs and turns, regulating the frequency size and direction of turns, to move in a favorable direction. Whether larvae use the same strategies wh...
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Significance To survive, an organism must adjust its behavior based upon past experiences. In Drosophila , aggression affects fitness as it ensures access to food and mating resources. Here, we show that upon repeated aggressive encounters, males adopt a winner or loser state that shows the qualities of persistence and generalization. Winning is pe...
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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...
Preprint
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Nervous systems across the animal kingdom have the ability to select appropriate actions and sequences of actions in response to sensory cues. The circuit mechanisms by which nervous systems achieve choice, stability and transitions between behaviors are still incompletely understood. To identify neurons and brain areas involved in controlling thes...
Article
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...
Article
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 ran...
Article
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. We reconstructed one such circuit at synaptic resolution, the $\textit{Drosophila}$ larval mushroom body, and found that most Kenyon cells int...
Article
Full-text available
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...
Preprint
Full-text available
Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higherorder circuit supporting associative memory has not been previously available. We reconstructed one such circuit at synaptic resolution, the Drosophila larval mushroom body, and found that most Kenyon cells integrate rando...
Article
Full-text available
The insect juvenile hormone receptor is a basic helix-loop-helix (bHLH), Per-Arnt-Sim (PAS) domain protein, a novel type of hormone receptor. In higher flies like Drosophila, the ancestral receptor germ cell-expressed (gce) gene has duplicated to yield the paralog Methoprene-tolerant (Met). These paralogous receptors share redundant function during...
Preprint
Full-text available
Visual systems transduce, process and transmit light-dependent environmental cues. Computation of visual features depends on the types of photoreceptor neurons (PR) present, the organization of the eye and the wiring of the underlying neural circuit. Here, we describe the circuit architecture of the visual system of Drosophila larvae by mapping the...
Article
Full-text available
Insect nervous systems are proven and powerful model systems for neuroscience research with wide relevance in biology and medicine. However, descriptions of insect brains have suffered from a lack of a complete and uniform nomenclature. Recognising this problem the Insect Brain Name Working Group produced the first agreed hierarchical nomenclature...
Data
PDF Neuron Atlas - Morphology and connectivity of reconstructed neurons. Reconstructions of (A) hugin-PC, (B) hugin-VNC, (C) hugin-RG, (D) hugin-PH neurons, (E) insulin-producing cells (IPCs), (F) DH44-producing cells, (G) DMS-producing cells, (H) antennal nerve (AN) sensory neurons as clustered in Figure 6, (I) abdominal nerve sensory neurons, (J)...
Data
Blender 3D Neuron Atlas – Morphology of reconstructed neurons as Blender file. To view, please download Blender (www.blender.org). Reconstructed neurons are sorted into layers: hugin neurons (1), mNSCs (2), sensory neurons (3), interneurons (4) and mesh of the larval brain (5, hidden by default). Neuron names contain id (e.g. #123456) to allow comp...
Article
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NeuromedinU is a potent regulator of food intake and activity in mammals. In Drosophila, neurons producing the homologous neuropeptide hugin regulate feeding and locomotion in a similar manner. Here, we use EM-based reconstruction to generate the entire connectome of hugin-producing neurons in the Drosophila larval CNS. We demonstrate that hugin ne...
Article
Full-text available
NeuromedinU is a potent regulator of food intake and activity in mammals. In Drosophila, neurons producing the homologous neuropeptide hugin regulate feeding and locomotion in a similar manner. Here, we use EM-based reconstruction to generate the entire connectome of hugin-producing neurons in the Drosophila larval CNS. We demonstrate that hugin ne...
Article
Even a simple sensory stimulus can elicit distinct innate behaviors and sequences. During sensorimotor decisions, competitive interactions among neurons that promote distinct behaviors must ensure the selection and maintenance of one behavior, while suppressing others. The circuit implementation of these competitive interactions is still an open qu...
Article
Even a simple sensory stimulus can elicit distinct innate behaviors and sequences. During sensorimotor decisions, competitive interactions among neurons that promote distinct behaviors must ensure the selection and maintenance of one behavior, while suppressing others. The circuit implementation of these competitive interactions is still an open qu...
Preprint
Full-text available
NeuromedinU is a potent regulator of food intake and activity in mammals. In Drosophila , neurons producing the homologous neuropeptide hugin regulate feeding and locomotion in a similar manner. Here, we use EM-based reconstruction to generate the entire connectome of hugin-producing neurons in the Drosophila larval CNS. We demonstrate that hugin n...
Article
Full-text available
(Neuron 91, 615–628; August 3, 2016) We regret and hereby correct the omission of Richard D. Fetter as an author, who performed sample preparation, serial sectioning and electron microscopy imaging of the whole Drosophila larval central nervous system, making possible the subsequent neuron reconstructions and synapse annotations of larval premotor...
Article
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We use Drosophila larval locomotion as a model to elucidate the working principles of motor circuits. Larval locomotion is generated by rhythmic and sequential contractions of body-wall muscles from the posterior to anterior segments, which in turn are regulated by motor neurons present in the corresponding neuromeres. Motor neurons are known to re...
Article
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Locomotor systems generate diverse motor patterns to produce the movements underlying behavior, requiring that motor neurons be recruited at various phases of the locomotor cycle. Reciprocal inhibition produces alternating motor patterns; however, the mechanisms that generate other phasic relationships between intrasegmental motor pools are unknown...
Article
It is unclear how regulatory genes establish neural circuits that compose sex-specific behaviors. The Drosophila melanogaster male courtship song provides a powerful model to study this problem. Courting males vibrate a wing to sing bouts of pulses and hums, called pulse and sine song, respectively. We report the discovery of male-specific thoracic...
Article
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Interindividual differences in neuronal wiring may contribute to behavioral individuality and affect susceptibility to neurological disorders. To investigate the causes and potential consequences of wiring variation in Drosophila melanogaster, we focused on a hemilineage of ventral nerve cord interneurons that exhibits morphological variability. We...
Data
No overt effect of 12A variability on wing song or escape from a looming stimulus. (A-G) Effects of genotype and rearing temperature on various parameters of wing song. In no case do both the T/CS and T/OR groups show a greater spread to the data than in both the CI and HI groups. This indicates that any potential effect of ectopic branching is sma...
Data
Raw Data—Voluntary takeoff delay. Data used in the creation of Fig 8A. Tab-delimited text. (TXT)
Data
Simulated effect of differentially mixed populations on distribution of behavior data. R simulation of how two populations (n = 40) that differ in the frequency of animals with the ectopic branch phenotype might look if the ectopic branch phenotype produces a 3σ effect. In conditions in which only 8% of animals harbor the ectopic branch phenotype (...