Reconstruction of motor control circuits in adult<i>Drosophila</i>using automated transmission electron microscopy

Maniates-Selvin, Jasper T.; Hildebrand, David G. C.; Graham, Brett J.; Kuan, Aaron T.; Thomas, Logan A.; Nguyen, Tri; Buhmann, Julia; Azevedo, Anthony W.; Shanney, Brendan L.; Funke, Jan; Tuthill, John C.; Lee, Wei-Chung Allen

doi:10.1101/2020.01.10.902478

Cited by 29 publications

(51 citation statements)

References 93 publications

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“…However, there is a dearth of information about how chordotonal mechanosensory neurons interface with downstream circuitry at the synaptic level. Our work here, along with two previous studies (Kim et al, 2020;Maniates-Selvin et al, 2020) reveal the near complete topography of mechanosensory neurons that make up the JO and the FeCO. This provides the foundation for rapid identification of neural circuitry that is postsynaptic to two different chordotonal organs.…”

Section: A Resource For Understanding How Sensory Topography Interfacsupporting

confidence: 74%

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Hampel

Eichler

Yamada

et al. 2020

Preprint

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Diverse subpopulations of mechanosensory neurons detect different mechanical forces and influence behavior. How these subpopulations connect with central circuits to influence behavior remains an important area of study. We previously discovered a neural circuit that elicits grooming of the Drosophila melanogaster antennae that is activated by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations and define how they interface with the circuit that elicits antennal grooming. We show that the subpopulations project to distinct zones in the brain and differ in their responses to mechanical stimulation of the antennae. Each subpopulation elicits grooming through direct synaptic connections with a single interneuron in the circuit, the dendrites of which span the different mechanosensory afferent projection zones. Thus, distinct JO subpopulations converge onto the same neural circuit to elicit a common behavioral response.The fruit fly (Drosophila melanogaster) Johnston's organ (JO) is a chordotonal organ in the antennae that can be studied to address this outstanding question. The JO detects diverse types of subpopulations are each known to consist of morphologically heterogeneous JON types that have not been completely described (Kamikouchi et al., 2006), we first define their morphological diversity by reconstructing major portions of each subpopulation from an EM volume of the fly brain (Zheng et al., 2018). We next produce transgenic driver lines that selectively target expression in each subpopulation. These lines enable us to visualize the distribution of the different subpopulations in the antennae and determine that they respond differently to mechanical stimuli. Optogenetic activation experiments confirm our previous finding that each JON subpopulation can elicit grooming of the antennae (Hampel et al., 2015). However, we report here that one of the subpopulations also elicits an avoidance response, whereas the other elicits wing flapping movements. Finally, by employing EM reconstructions and functional imaging experiments, we determine that JONs within each subpopulation are synaptically and functionally connected with the antennal command circuit through the same interneuron (aBN1). These results provide a comprehensive description of the topography of the JO, and reveal how different JON subpopulations whose projections occupy different points in topographical space can converge on the same neural circuit to elicit a similar behavioral response. Results and discussion Electron microscopy-based reconstruction of different JON subpopulationsWe first sought to define the morphological diversity of the neurons within each JON subpopulation as a prerequisite for understanding how the subpopulations interface with the antennal command circuit. JONs project from the antennae through the antennal nerve into a region of the SEZ called the antennal mechanosensory and motor ce...

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Section: A Resource For Understanding How Sensory Topography Interfacsupporting

confidence: 74%

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Hampel

Eichler

Yamada

et al. 2020

Preprint

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“…Drosophila is a uniquely powerful model system for this kind of circuit dissection: recent efforts have identified and mapped the majority of leg motor neurons (Azevedo et al, 2019;Baek and Mann, 2009;Brierley et al, 2012) and leg sensory neurons (Mamiya et al, 2018;Tsubouchi et al, 2017;Tuthill and Wilson, 2016). Additionally, serial-section EM imaging of the VNC will enable precise reconstructions of the neural connectome (Maniates-Selvin et al, 2020). This solid anatomical framework, coupled with detailed functional investigations of VNC cell-types such as the one undertaken in this study, will deepen our understanding of the fundamental computations underlying proprioception.…”

Section: Discussionmentioning

confidence: 94%

“…1A). The FeCO is the largest proprioceptive organ in the fruit fly, Drosophila melanogaster (Meigen, 1830), and its 152 neurons can be divided into at least three anatomically distinct subtypes: the claw, hook, and club neurons (Mamiya et al, 2018;Maniates-Selvin et al, 2020;Pacureanu et al, 2019;Phillis et al, 1996). Each subtype encodes different kinematic features of the femur-tibia joint: claw neurons encode tibia position (flexion or extension; Fig.…”

Section: Introductionmentioning

confidence: 99%

Central processing of leg proprioception inDrosophila

Agrawal

Dickinson

Sustar

et al. 2020

Preprint

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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 circuits in Drosophila that process proprioceptive information from the fly leg. We identify three cell-types from distinct developmental lineages that are positioned to receive input from proprioceptor subtypes encoding tibia position, movement, and vibration. 13Bα neurons encode femur-tibia joint angle and mediate postural changes in tibia position. 9Aα neurons also drive changes in leg posture, but encode a combination of directional movement, high frequency vibration, and joint angle. Activating 10Bα neurons, which encode tibia vibration at specific joint angles, elicits pausing in walking flies. Altogether, our results reveal that central circuits integrate information across proprioceptor subtypes to construct complex sensorimotor representations that mediate diverse behaviors, including reflexive control of limb posture and detection of leg vibration.

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“…Comprehensive electron microscopy (EM) mapping of specific brain regions or whole nervous systems is transforming neuroscience (e.g. Zheng, et al, 2018;Maniates-Selvin, et al, 2020;Scheffer, et al, 2020) by providing anatomy at unparalleled resolution, near complete cell type coverage, and connectivity information. However, leveraging these new datasets to understand more than pure anatomy will be greatly facilitated by the ability to genetically target specific neurons and circuits.…”

Section: Introductionmentioning

confidence: 99%

A searchable image resource ofDrosophilaGAL4-driver expression patterns with single neuron resolution

Meissner

Dorman²,

Nern³

et al. 2020

Preprint

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Precise, repeatable genetic access to specific neurons via the GAL4/UAS system and related methods is a key advantage of Drosophila neuroscience. Neuronal targeting is typically documented using light microscopy of full GAL4 expression patterns, which mostly lack the single-cell resolution required for reliable cell type identification. Here we use stochastic GAL4 labeling with the MultiColor FlpOut approach to generate cellular resolution confocal images at large scale. We are releasing aligned images of 27,000 such adult central nervous systems.An anticipated use of this resource is to bridge the gap between electron microscopyidentified neurons and light microscopy-based intersectional genetic approaches such as the split-GAL4 system. Identifying the individual neurons that make up each GAL4 expression pattern improves the prediction of which GAL4 enhancer fragments best combine via split-GAL4 to target neurons of interest. To this end we have developed the NeuronBridge search tool, which matches these light microscope neuronal images to neurons in the recently published FlyEM hemibrain. This work thus provides a resource and search tool that will significantly enhance both the efficiency and efficacy of split-GAL4 targeting of EM-identified neurons and further advance Drosophila neuroscience.Meissner, et al., 2020Gen1 MCFO Phase 1 release

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Reconstruction of motor control circuits in adultDrosophilausing automated transmission electron microscopy

Cited by 29 publications

References 93 publications

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Central processing of leg proprioception inDrosophila

A searchable image resource ofDrosophilaGAL4-driver expression patterns with single neuron resolution

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