The natverse: a versatile computational toolbox to combine and analyse neuroanatomical data

Manton, James D.; Bates, Alexander Shakeel; Jagannathan, Sridhar R.; Costa, Marta; Schlegel, Philipp; Rohlfing, Torsten; Jefferis, Gregory

doi:10.1101/006353

Cited by 32 publications

(38 citation statements)

References 139 publications

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“…The Jacobs archive in http://neuromorpho.org, for example, had over one million downloads of traced neurons in 2015 (Ascoli, ) and, at the time of this publication, over two million. As noted by Manton et al (), who recently examined 3,174 neurons across 24 different species from the Jacobs http://neuromorpho.org archive, it is particularly important for cross‐species comparisons that neurons be acquired with the same methodology. Beyond morphology, other studies have examined dendritic computation patterns and topological factors across species using the same Jacobs archive (Kirch & Gollo, ).…”

Section: Resultsmentioning

confidence: 99%

Comparative neocortical neuromorphology in felids: African lion, African leopard, and cheetah

Nguyen

Uchida

Warling

et al. 2019

J of Comparative Neurology

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The present study examines cortical neuronal morphology in the African lion (Panthera leo leo), African leopard (Panthera pardus pardus), and cheetah (Acinonyx jubatus jubatus). Tissue samples were removed from prefrontal, primary motor, and primary visual cortices and investigated with a Golgi stain and computer‐assisted morphometry to provide somatodendritic measures of 652 neurons. Although neurons in the African lion were insufficiently impregnated for accurate quantitative dendritic measurements, descriptions of neuronal morphologies were still possible. Qualitatively, the range of spiny and aspiny neurons across the three species was similar to those observed in other felids, with typical pyramidal neurons being the most prominent neuronal type. Quantitatively, somatodendritic measures of typical pyramidal neurons in the cheetah were generally larger than in the African leopard, despite similar brain sizes. A MARsplines analysis of dendritic measures correctly differentiated 87.4% of complete typical pyramidal neurons between the African leopard and cheetah. In addition, unbiased stereology was used to compare the soma size of typical pyramidal neurons (n = 2,238) across all three cortical regions and gigantopyramidal neurons (n = 1,189) in primary motor and primary visual cortices. Both morphological and stereological analyses indicated that primary motor gigantopyramidal neurons were exceptionally large across all three felids compared to other carnivores, possibly due to specializations related to the felid musculoskeletal systems. The large size of these neurons in the cheetah which, unlike lions and leopards, does not belong to the Panthera genus, suggests that exceptionally enlarged primary motor gigantopyramidal neurons evolved independently in these felid species.

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Section: Resultsmentioning

confidence: 99%

Comparative neocortical neuromorphology in felids: African lion, African leopard, and cheetah

Nguyen

Uchida

Warling

et al. 2019

J of Comparative Neurology

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“…We then assigned odour scenes ( Figure S7) to each community based on the glomeruli innervated by their PNs ( Figure 3I) [43,44]. Community 2, for example, mainly consists of PNs that innervate pheromoneresponsive glomeruli DA1, DL3, DC3, VA1v, matching a previously described pheromonal LH compartment ( Figure S3C) [38,39]. Other communities show equally distinct fingerprints suggesting a certain degree of specialisation present in the topology of the network.…”

Section: Axo-axonic Connections Are Widespread Between Olfactory Projmentioning

confidence: 91%

“…The LH can be roughly compartmentalised according to biological valence [5,[38][39][40][41]. Seeing that most of the axoaxonic PN→PN synapses occur in the LH, we asked whether we could find a similar organisation within the PN→PN network.…”

Section: Axo-axonic Connections Are Widespread Between Olfactory Projmentioning

confidence: 99%

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Complete connectomic reconstruction of olfactory projection neurons in the fly brain

Bates

Schlegel

Roberts

et al. 2020

Preprint

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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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“…The connectivity and graph widgets in CATMAID were used to analyse and visualise connectivity between traced skeletons. R packages from the natverse collection (http://natverse.org/) [55] were used to plot traced skeletons and analyse their morphology. Custom R and Python scripts were used to perform additional analysis, as described below.…”

Section: Analysis and Representation Of Traced Skeletonsmentioning

confidence: 99%

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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The natverse: a versatile computational toolbox to combine and analyse neuroanatomical data

Cited by 32 publications

References 139 publications

Comparative neocortical neuromorphology in felids: African lion, African leopard, and cheetah

Comparative neocortical neuromorphology in felids: African lion, African leopard, and cheetah

Complete connectomic reconstruction of olfactory projection neurons in the fly brain

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

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