Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adult<i>Drosophila</i>brain

Marin, Elizabeth C.; Roberts, Ruairí J.V.; Büld, Laurin; Theiß, M.; Pleijzier, Markus William; Sarkissian, Tatevik; Laursen, Willem J.; Turnbull, Robert; Schlegel, Philipp; Bates, Alexander Shakeel; Li, Feng; Landgraf, Matthias; Costa, Marta; Bock, Davi D.; Garrity, Paul; Jefferis, Gregory S.X.E.

doi:10.1101/2020.01.20.912709

Cited by 8 publications

(8 citation statements)

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“…We acquire the majority of neurotransmitter to neuron assignments used for training and evaluation from published reconstructions in the full adult fly brain (FAFB) dataset (Bates et al, 2020;Dolan et al, 2018;Felsenberg et al, 2018;Frechter et al, 2019;Huoviala et al, 2018;Dolan et al, 2019;Marin et al, 2020;Sayin et al, 2019;Turner-Evans et al, 2019;Zheng et al, 2018), as well as unpublished but identified neuron reconstructions offered by the FAFB community (see acknowledgements). In these studies, the authors had already linked some of their reconstructed cell types to immunohistochemical data (Aso et al, 2014;Bräcker et al, 2013;Busch et al, 2009;Davis et al, 2018;Dolan et al, 2019;Ito et al, 2013;Lai et al, 2008;Okada et al, 2009;Shinomiya et al, 2015;Tanaka et al, 2012;Wilson and Laurent, 2005).…”

Section: Data Acquisitionmentioning

confidence: 99%

Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster

Eckstein

Bates

et al. 2020

Preprint

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High-resolution electron microscopy (EM) of nervous systems enables the reconstruction of neural circuits at the level of individual synaptic connections. However, for invertebrates, such as Drosophila melanogaster, it has so far been unclear whether the phenotype of neurons or synapses alone is sufficient to predict specific functional properties such as neurotransmitter identity. Here, we show that in Drosophila melanogaster artificial convolutional neural networks can confidently predict the type of neurotransmitter released at a synaptic site from EM images alone. The network successfully discriminates between six types of neurotransmitters (GABA, glutamate, acetylcholine, serotonin, dopamine, and octopamine) with an average accuracy of 87% for individual synapses and 94% for entire neurons, assuming each neuron expresses only one neurotransmitter. This result is surprising as there are often no obvious cues in the EM images that human observers can use to predict neurotransmitter identity. We apply the proposed method to quantify whether, similar to the ventral nervous system (VNS), all hemilineages in the Drosophila melanogaster brain express only one fast acting transmitter within their neurons. To test this principle, we predict the neurotransmitter identity of all identified synapses in 89 hemilineages in the Drosophila melanogaster adult brain. While the majority of our predictions show homogeneity of fast-acting neurotransmitter identity within a single hemilineage, we identify a set of hemilineages that express two fast-acting neurotransmitters with high statistical significance. As a result, our predictions are inconsistent with the hypothesis that all neurons within a hemilineage express the same fast-acting neurotransmitter in the brain of Drosophila melanogaster.

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Section: Data Acquisitionmentioning

confidence: 99%

Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster

Eckstein

Bates

et al. 2020

Preprint

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108

134

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“…We began by asking if the connectivity of the CSDn to individual PNs differs across the AL and LH as both the CSDn and PNs span both brain regions. Previously published PN reconstructions [25, 50, 67] were grouped into three subtypes based on whether they were uniglomerular (uPN) or multiglomerular (mPN), and the AL tract along which the mPNs project, either mALT or mlALT [50]. In addition to the AL tract along which they project, mPNs functionally differ from each other in terms of the transmitter they express with mALT mPNs being cholinergic and mlALT mPNs being GABAergic [50, 68–70].…”

Section: Resultsmentioning

confidence: 99%

The wiring logic of an identified serotonergic neuron that spans sensory networks

Coates

Calle-Schuler

Helmick

et al. 2020

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19Serotonergic neurons modulate diverse physiological and behavioral processes in a 20 context-dependent manner, based on their complex connectivity. However, their 21 connectivity has not been comprehensively explored at a single-cell resolution. Using a 22 whole-brain EM dataset we determined the wiring logic of a broadly projecting 23 serotonergic neuron (the "CSDn") in Drosophila. Within the antennal lobe (AL; first-order 24 olfactory region), the CSDn receives glomerulus-specific input and preferentially targets 25 distinct local interneuron subtypes. Furthermore, the wiring logic of the CSDn differs 26 between olfactory regions. The CSDn innervates the AL and lateral horn (LH), yet does 27 not maintain the same synaptic relationship with individual projection neurons that also 28 span both regions. Consistent with this, the CSDn has more distributed connectivity in 29 the LH relative to the AL, preferentially synapsing with principal neuron types based on 30 presumptive transmitter content. Lastly, we identify protocerebral neurons that provide 31 abundant synaptic input to the CSDn. Our study demonstrates how an individual 32 modulatory neuron can interact with local networks and integrate input from non-33 olfactory sources. 35Introduction 36 Every neural network receives modulatory input from a variety of sources [1, 2], 37 and in some cases from heterogeneous populations of neurons that release the same 38 modulatory transmitter [3][4][5]. In mammals, one ubiquitous neuromodulator, serotonin, is 39 released by tens of thousands to hundreds of thousands of neurons which originate in 40 the raphe nuclei and project throughout the brain [6, 7]. Serotonergic raphe neurons are 41 highly diverse in their projections, connectivity, and electrophysiological properties, and 42 2 are implicated in a wide breadth of behaviors and physiological processes [4,[8][9][10][11][12][13][14][15][16]. 43 Further, the raphe system receives monosynaptic input from up to 80 anatomical areas 44 [8, 9]. As a result, a significant amount of work has focused on disentangling the 45 functional and behavioral roles of serotonergic neurons. Several recent studies have 46 suggested that serotonergic raphe neurons may be organized into functional 47 subpopulations based on neuroanatomy, electrophysiology, and behavior [4, 12,[17][18][19][20][21]. 48For example, two parallel sub-systems of serotonergic raphe neurons collateralize 49 complimentarily and are both activated by reward, yet have opposing responses to 50 aversive stimuli and promote distinct behaviors [18]. Sparse neuron reconstructions in 51 mice show that a single serotonin neuron can interconnect the olfactory bulb, piriform 52 cortex, and anterior olfactory nucleus [19], demonstrating that a single serotonergic 53 neuron can arborize several processing stages within the same sensory modality. Thus, 54 determining the precise patterns of connectivity of single serotonergic neurons within 55 and across the brain regions will be critical for understanding t...

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“…Preferential connectivity of JONs within a particular subpopulation has also been shown with the JO-A and -B neurons (Kim et al, 2020). This type of connectivity among sensory neurons is an emerging theme that is increasingly being described in sensory neurons across modalities (Horne et al, 2018;Marin et al, 2020;Miroschnikow et al, 2018;Tobin et al, 2017). However, the functional significance of this type of connectivity remains unclear.…”

Section: Jon Axons Make Synaptic Connections With Each Othermentioning

confidence: 96%

“…The algorithm would occasionally create false splits. Therefore, the tracer resolved these false splits by manually assembling the fragments as previously described (Marin et al, 2020). This approach enabled us to semi-automatically annotate the major branches of each neuron, but not the fine branches and synaptic sites.…”

Section: Neural Circuit Reconstructions From An Em Volumementioning

confidence: 99%

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

Hampel

Eichler

Yamada

et al. 2020

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

Cited by 8 publications

References 59 publications

Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster

Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster

The wiring logic of an identified serotonergic neuron that spans sensory networks

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

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