NBLAST: Rapid, Sensitive Comparison of Neuronal Structure and Construction of Neuron Family Databases

Costa, Marta; Manton, James D.; Ostrovsky, Aaron D.; Prohaska, Steffen; Jefferis, Gregory S.X.E.

doi:10.1016/j.neuron.2016.06.012

Cited by 280 publications

(286 citation statements)

References 73 publications

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“…Briefly, in Drosophila , as in other insects, the gross morphology of many neurons is stereotyped and individual neurons are uniquely identifiable on the basis of morphology 61-63 . Furthermore, the nervous system in insects is largely bilaterally symmetrical and homologous neurons are reproducibly found on the left and the right side of the animal.…”

Section: Methodsmentioning

confidence: 99%

The complete connectome of a learning and memory centre in an insect brain

Eichler

Litwin-Kumar

et al. 2017

Nature

489

726

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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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Section: Methodsmentioning

confidence: 99%

The complete connectome of a learning and memory centre in an insect brain

Eichler

Litwin-Kumar

et al. 2017

Nature

489

726

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“…S1E'''). Morphological clustering with NBLAST [33] of unilateral VP sensory neurons paired the simpler VP3 TRNs on each side with one another, within the larger VP3 TRN group (Fig. S2A), implying that they are of the same type and distinct from the complex VP3 TRNs.…”

Section: Sensory Neurons Define Two Novel Glomeruli In the Ventropostmentioning

confidence: 96%

Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adultDrosophilabrain

Marin

Roberts

Büld

et al. 2020

Preprint

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HIGHLIGHTS• Two novel thermo/hygrosensory glomeruli in the fly antennal lobe • First complete set of thermosensory and hygrosensory projection neurons • First connectome for a thermosensory centre, the lateral accessory calyx • Novel third order neurons, including a link to the circadian clock SUMMARY (250):Animals exhibit innate and learned preferences for temperature and humidity -conditions critical for their survival and reproduction. Here, we leveraged a whole adult brain electron microscopy volume to study the circuitry associated with antennal thermosensory and hygrosensory neurons, which target specific ventroposterior (VP) glomeruli in the Drosophila melanogaster antennal lobe. We have identified two new VP glomeruli, in addition to the five known ones, and the projection neurons (VP PNs) that relay VP information to higher brain centres, including the mushroom body and lateral horn, seats of learned and innate olfactory behaviours, respectively. Focussing on the mushroom body lateral accessory calyx (lACA), a known thermosensory neuropil, we present a comprehensive connectome by reconstructing neurons downstream of heating-and coolingresponsive VP PNs. We find that a few lACA-associated mushroom body intrinsic neurons (Kenyon cells) solely receive thermosensory inputs, while most receive additional olfactory and thermo-or hygrosensory PN inputs in the main calyx. Unexpectedly, we find several classes of lACA-associated neurons that form a local network with outputs to other brain neuropils, suggesting that the lACA serves as a general hub for thermosensory circuitry. For example, we find DN1 pacemaker neurons that link the lACA to the accessory medulla, likely mediating temperature-based entrainment of the circadian clock. Finally, we survey strongly connected downstream partners of VP PNs across the protocerebrum; these include a descending neuron that receives input mainly from dry-responsive VP PNs, meaning that just two synapses might separate hygrosensory inputs from motor neurons in the nerve cord. (249) KEYWORDSThermosensation, hygrosensation, connectomics, antennal lobe, projection neuron, lateral accessory calyx, circadian clock Temperature and humidity are two interrelated environmental variables with dramatic effects on animal physiology and survival. Animals exhibit intrinsic species-specific preferences for the temperature and humidity levels compatible with their survival and reproduction [1]. However, these preferences can be modulated by state and experience; vinegar flies prefer higher levels of relative humidity when dehydrated [2], and nematodes starved at low humidity subsequently prefer higher humidities, and vice versa [3]. Temperature and/or humidity also cue essential behavioural programmes; for example, female mosquitoes use heat and humidity to locate warmblooded hosts for blood feeding [4,5], and temperature entrains the circadian clock in organisms from molds to mammals to drive daily rhythms of physiology and behaviour [6,7]. Whilst fundamental for survival, the neuronal mec...

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“…4 Every cell within a cluster appears to have a unique arborization and F I G U R E 4 The second mode of action of FruBM in the control of neural sex differentiation. 51 We cannot exclude the possibility that two neurons exhibiting a subtle structural difference within a cluster participate in distinct connections and thus distinct behavior, rather than forming redundant connections contributing to the improvement of safety factors of the system. fru-mutant males express femalespecific Lola-Q.…”

Section: Unsolved Issuesmentioning

confidence: 99%

“…For example, the 29 male mAL neurons registered in NBLAST are classified into four groups based on their neurite branching patterns, such that rigorous characterization of the fine branching might allow one to identify a single neuron in a cluster. 51 We cannot exclude the possibility that two neurons exhibiting a subtle structural difference within a cluster participate in distinct connections and thus distinct behavior, rather than forming redundant connections contributing to the improvement of safety factors of the system. How these subtle differences in the neurite pattern are produced are elusive.…”

Section: Unsolved Issuesmentioning

confidence: 99%

The mode of action of Fruitless: Is it an easy matter to switch the sex?

Sato

Yamamoto

2019

Genes Brain and Behavior

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The fruitless (fru) locus was originally defined by a male sterile mutation that promotes male‐to‐male courtship while suppressing male‐to‐female courtship in Drosophila melanogaster. The fru promoter‐1 pre‐RNA generates a set of BTB‐zinc finger family FruM proteins expressed exclusively in the male neurons, leading to the formation of sexual dimorphisms in neurons via male‐specific neuroblast proliferation, male‐specific neural survival, male‐specific neuritegenesis or male‐specific arbor patterning. Such a wide spectrum of phenotypic effects seems to result from chromatin modifications, in which FruBM recruits Bonus, Histone deacetylase 1 (HDAC1) and/or Heterochromatin protein 1a (HP1a) to ~130 target sites. One established FruBM transcriptional target is the axon guidance protein gene robo1. Multiple transcriptional regulator‐binding sites are nested around the FruBM‐binding site, and mediate sophisticated modulation of the repressor activity of FruBM. FruBM also binds to the Lola‐Q transcriptional repressor to protect it from proteasome‐dependent degradation in male but not female neurons as FruBM exists only in male neurons, leading to the formation of sexually dimorphic neural structures. These findings shed light on the multilayered network of transcription regulation orchestrated by the master regulator FruBM.

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NBLAST: Rapid, Sensitive Comparison of Neuronal Structure and Construction of Neuron Family Databases

Cited by 280 publications

References 73 publications

The complete connectome of a learning and memory centre in an insect brain

The complete connectome of a learning and memory centre in an insect brain

Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adultDrosophilabrain

The mode of action of Fruitless: Is it an easy matter to switch the sex?

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