Neurotransmitter identity is acquired in a lineage-restricted manner in the Drosophila CNS

Lacin, Haluk; Chen, Hui Min; Long, Xi; Singer, Robert H.; Lee, Tzumin; Truman, James W.

doi:10.7554/elife.43701

Cited by 105 publications

(207 citation statements)

References 71 publications

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“…S3B). We hypothesize that these 18 bundles correspond to developmental lineages, which typically have their primary neurites bundled together (Lacin et al, 2019). Five of these bundles totaling 42 neurons exited the VNC through the ProLN (Fig.…”

Section: Cell Type-specific Clustering Of Sensory and Motor Neuron Axonsmentioning

confidence: 97%

Reconstruction of motor control circuits in adultDrosophilausing automated transmission electron microscopy

Maniates-Selvin

Hildebrand

Graham

et al. 2020

Preprint

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Many animals use coordinated limb movements to interact with and navigate through the environment. To investigate circuit mechanisms underlying locomotor behavior, we used serial-section electron microscopy (EM) to map synaptic connectivity within a neuronal network that controls limb movements. We present a synapse-resolution EM dataset containing the ventral nerve cord (VNC) of an adult female Drosophila melanogaster. To generate this dataset, we developed GridTape, a technology that combines automated serial-section collection with automated high-throughput transmission EM. Using this dataset, we reconstructed 507 motor neurons, including all those that control the legs and wings. We show that a specific class of leg sensory neurons directly synapse onto the largest-caliber motor neuron axons on both sides of the body, representing a unique feedback pathway for fast limb control. We provide open access to the dataset and reconstructions registered to a standard atlas to permit matching of cells between EM and light microscopy data. We also provide GridTape instrumentation designs and software to make large-scale EM data acquisition more accessible and affordable to the scientific community.

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Section: Cell Type-specific Clustering Of Sensory and Motor Neuron Axonsmentioning

confidence: 97%

Reconstruction of motor control circuits in adultDrosophilausing automated transmission electron microscopy

Maniates-Selvin

Hildebrand

Graham

et al. 2020

Preprint

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“…To assign putative neurotransmitters, we assumed that neurons within the same hemi-lineage express the same neurotransmitter(s). This has been shown to be true in the ventral nerve cord [24]. Most extant transmitter data is based on GAL4 driver lines which can have incomplete (i.e.…”

Section: Pn Types and Putative Neurotransmittersmentioning

confidence: 98%

“…We found 346 neurons with dendrites in the right AL and axonal projections to other neuropils ( Figure 1C, see Methods). We crossreferenced these PNs with extant data [22,23], linking neurons to their developmental hemilineages and putative neurotransmitter expression ( Figure S1A; Supplemental Data; see Methods) [24][25][26][27][28].…”

Section: A Full Account Of Olfactory Projection Neurons Connecting Sementioning

confidence: 99%

Complete connectomic reconstruction of olfactory projection neurons in the fly brain

Bates

Schlegel

Roberts

et al. 2020

Preprint

218

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Nervous systems contain sensory neurons, local neurons, projection neurons and motor neurons. To understand how these building blocks form whole circuits, we must distil these broad classes into neuronal cell types and describe their network connectivity. Using an electron micrograph dataset for an entire Drosophila melanogaster brain, we reconstruct the first complete inventory of olfactory projections connecting the antennal lobe, the insect analogue of the mammalian olfactory bulb, to higher-order brain regions in an adult animal brain. We then connect this inventory to extant data in the literature, providing synaptic-resolution 'holotypes' both for heavily investigated and previously unknown cell types. Projection neurons are approximately twice as numerous as reported by light level studies; cell types are stereotyped, but not identical, in cell and synapse numbers between brain hemispheres. The lateral horn, the insect analogue of the mammalian cortical amygdala, is the main target for this olfactory information and has been shown to guide innate behaviour. Here, we find new connectivity motifs, including: axo-axonic connectivity between projection neurons; feedback and lateral inhibition of these axons by local neurons; and the convergence of different inputs, including non-olfactory inputs and memory-related feedback onto lateral horn neurons. This differs from the configuration of the second most prominent target for olfactory projection neurons: the mushroom body calyx, the insect analogue of the mammalian piriform cortex and a centre for associative memory. Our work provides a complete neuroanatomical platform for future studies of the adult Drosophila olfactory system. Highlights• First complete parts list for second-order neurons of an adult olfactory system • Quantification of left-right stereotypy in cell and synapse number • Axo-axonic connections form hierarchical communities in the lateral horn • Local neurons and memory-related feedback target projection neuron axons 149 197 346 Figure 1: Second-order olfactory projection neurons. A Layout of the mammalian olfactory system. B The olfactory system in fruit flies shares similarities with that of mammals. C Second-order olfactory projection neurons (PNs) in all antennal lobe tracts (ALT) were reconstructed from a serial section transmission electron microscopy (ssTEM) volume of an entire fly brain. Scale bar represents 1 micron. D Exemplary sparse (left) and broad (right) PN. Dendrites used for classification in blue. E PNs were classified as uni-(uPN) or multiglomerular (mPN) projection neurons based on the sparseness of their glomerular innervation (see also Figure S1). F PN counts by class and neurotransmitter. G Comparison of right-(RHS) vs left-hand-side (LHS) cell counts for 58 of the 78 uPN types. H Scaling of the olfactory system from larval to adult D. melanogaster. Bates, Schlegel et al. 2 / 31

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“…This principle provides a useful framework for understanding the organization and function of motor circuits that flexibly control a wide range of fly behaviors, from walking to aggression to courtship. Studies of motor control in the fly VNC are now possible thanks to an increasing catalog of genetically-identified cell types (Lacin et al, 2019;Shepherd et al, 2019, Namiki et al, 2018, connectomic reconstruction with serial-section EM and the ability to image from VNC neurons in walking flies (Chen et al, 2018). We anticipate that Drosophila will provide a useful complement to other model organisms in understanding the neural basis of flexible motor control.…”

Section: Discussionmentioning

confidence: 99%

A size principle for leg motor control inDrosophila

Azevedo

Dickinson

Gurung

et al. 2019

Preprint

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To move the body, the brain must precisely coordinate patterns of activity among diverse populations of motor neurons. In many species, including vertebrates, the motor neurons innervating a given muscle fire in a specific order that is determined by a gradient of cellular size and electrical excitability. This hierarchy allows premotor circuits to recruit motor neurons of increasing force capacity in a task-dependent manner. However, it remains unclear whether such a size principle also applies to species with more compact motor systems, such as the fruit fly, Drosophila melanogaster, which has just 53 motor neurons per leg. Using in vivo calcium imaging and electrophysiology, we found that genetically-identified motor neurons controlling flexion of the fly tibia exhibit a gradient of anatomical, physiological, and functional properties consistent with the size principle. Large, fast motor neurons control high force, ballistic movements while small, slow motor neurons control low force, postural movements. Intermediate neurons fall between these two extremes. In behaving flies, motor neurons are recruited in order from slow to fast. This hierarchical organization suggests that slow and fast motor neurons control distinct motor regimes. Indeed, we find that optogenetic manipulation of each motor neuron type has distinct effects on the behavior of walking flies.

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Neurotransmitter identity is acquired in a lineage-restricted manner in the Drosophila CNS

Cited by 105 publications

References 71 publications

Reconstruction of motor control circuits in adultDrosophilausing automated transmission electron microscopy

Reconstruction of motor control circuits in adultDrosophilausing automated transmission electron microscopy

Complete connectomic reconstruction of olfactory projection neurons in the fly brain

A size principle for leg motor control inDrosophila

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