Multimodal sensory processing in
            <i>Caenorhabditis elegans</i>

Metaxakis, Athanasios; Petratou, Dionysia; Tavernarakis, Nektarios

doi:10.1098/rsob.180049

Cited by 42 publications

(38 citation statements)

References 107 publications

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“…1b,c; Extended Data Fig. 2a,b; [32][33][34][35][36][37][38][39] ), consistent with behavioral and connectomic studies 10,19,20 . The multigranular outputs of the DC/C-PHATE results enabled understanding of the cell-cell interactions within the context of functional circuits, and the functional circuits within the context of the larger bundles of the neuropil.Comparisons of the modularity score, a measure of cluster robustness 40,41 , was highest when the majority of neurites were grouped into four super-clusters ( Fig.…”

supporting

confidence: 82%

Structural and developmental principles of neuropil assembly inC. elegans

Moyle

Barnes

Kuchroo

et al. 2020

Preprint

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To visualize DC cluster relationships we developed C-PHATE, an extension of PHATE 30 capable of generating a 3D representation of the multigranular structures in the DC hierarchical tree ( Fig. 1a,b; see Methods). Quantitative comparisons of DC/C-PHATE results revealed similar clustering behaviors between the two separately analyzed nervering reconstructions (Adjusted Rand Index (ARI) of 0.7; Extended Data Fig. 1a,b), consistent with the long-accepted qualitative descriptions of the stereotyped structure for the C. elegans nerve ring 3,31 , and recent analyses of neurite adjacencies 22 . Examination of the cluster patterns through the iterations of DC revealed known cell-cell interactions and behavioral circuits ( Fig. 1b,c; Extended Data Fig. 2a,b; [32][33][34][35][36][37][38][39] ), consistent with behavioral and connectomic studies 10,19,20 . The multigranular outputs of the DC/C-PHATE results enabled understanding of the cell-cell interactions within the context of functional circuits, and the functional circuits within the context of the larger bundles of the neuropil.Comparisons of the modularity score, a measure of cluster robustness 40,41 , was highest when the majority of neurites were grouped into four super-clusters ( Fig. 1b; Extended Data Fig. 1a,b; Supplemental Video 1,2; see Methods). Overlaying our analysis of these four super-clusters (see Methods) onto the anatomy of the nerve ring revealed that they correspond to four distinct and tightly grouped bundles within the greater neuropil, circling the pharynx isthmus and stacked along the anterior-posterior axis of the animal. These clusters are herein called S1, S2, S3 and S4 for Stratum 1 etc. (Fig. 1c; Extended Data Fig. 1c-h; Supplemental Video 3 show details of these structures and single-cell identities). The stratified organization of the nerve ring neuropil, resolved here at single neurite level, is reminiscent of laminar organizations in the Drosophila nervous system 42,43 , and in the vertebrate retina and the brain cortex 44,45 .We observed that not all computationally clustered neurites followed simple bundled paths through the neuropil. In Strata 1 (S1), 32 anterior sensory neurons project perpendicular to the nerve ring bundle before making a 180º curl and returning to the anterior limits of the neuropil, where they terminate as synaptic endplates (Fig. 1d; Extended Data Fig. 3a-d; 3,46 ). These uniquely shaped S1 neurons looped at the borders of the S2/S3/S4 bundles. The anterior loops encase ~90% of S2, and the posterior loops encase ~84% of S3 and 100% of S4 ( Fig. 1d-g; Extended Data Fig. 3e-k ; SupplementalVideo 5; Supplemental Table 1). We found that the 32 axons form a six-fold symmetrical honeycomb structure along the neuropil's arc, creating a scaffold that encapsulates the different strata ( Fig. 1g; Extended Data Fig. 3e-h; Supplemental Video 4).The architecture of the neuropil reflects functional segregation of distinct sensory information streams and motor outputs.C. elegans neurons can be divided into three categories ...

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supporting

confidence: 82%

Structural and developmental principles of neuropil assembly inC. elegans

Moyle

Barnes

Kuchroo

et al. 2020

Preprint

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“…Multisensory integration in C. elegans falls into two broad categories: co-exposure to two distinct stimuli, aversive and attractive, or exposure to one stimuli in conjunction with an environmental indicator, both of which can be tested via avoidance assays [80,81,82]. Furthermore, with only sixteen pairs of chemosensory neurons, neuronal ablation techniques such as the laser ablation method as well as genetic ablations have become effective tools for understanding the diverse roles of individual sensory neurons within the realm of the connectome [83,84].…”

Section: Analysis Of the Functional Connectomementioning

confidence: 99%

Novel Technological Advances in Functional Connectomics in C. elegans

DiLoreto

Chute

Bryce

et al. 2019

JDB

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The complete structure and connectivity of the Caenorhabditis elegans nervous system (“mind of a worm”) was first published in 1986, representing a critical milestone in the field of connectomics. The reconstruction of the nervous system (connectome) at the level of synapses provided a unique perspective of understanding how behavior can be coded within the nervous system. The following decades have seen the development of technologies that help understand how neural activity patterns are connected to behavior and modulated by sensory input. Investigations on the developmental origins of the connectome highlight the importance of role of neuronal cell lineages in the final connectivity matrix of the nervous system. Computational modeling of neuronal dynamics not only helps reconstruct the biophysical properties of individual neurons but also allows for subsequent reconstruction of whole-organism neuronal network models. Hence, combining experimental datasets with theoretical modeling of neurons generates a better understanding of organismal behavior. This review discusses some recent technological advances used to analyze and perturb whole-organism neuronal function along with developments in computational modeling, which allows for interrogation of both local and global neural circuits, leading to different behaviors. Combining these approaches will shed light into how neural networks process sensory information to generate the appropriate behavioral output, providing a complete understanding of the worm nervous system.

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“…Multiple sensory inputs or physiological states such as oxygen level, odors, tastes, mechanosensation, pain, and hunger must be integrated in order to evaluate the environment and come to a decision. These cues are most likely integrated in the interneurons of C. elegans, which are downstream of the sensory neurons (Metaxakis et al, 2018;Summers et al, 2015;Wilson et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

TRPM channels mediate learned pathogen avoidance following intestinal distention

Filipowicz

Aballay

2020

Preprint

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Upon exposure to harmful microorganisms, hosts engage in protective molecular and behavioral immune responses, both of which are ultimately regulated by the nervous system. Using the nematode Caenorhabditis elegans, we show that ingestion of E. faecalis leads to a fast pathogen avoidance behavior that results in aversive learning. We have identified multiple sensory mechanisms involved in the regulation of avoidance of E. faecalis, including the GPCR NPR-1-dependent oxygen-sensing pathway, an ASE neuron-dependent pathway, and an AWB and AWC neuron-dependent pathway. Colonization of the anterior part of the intestine by E. faecalis leads to AWB and AWC mediated olfactory aversive learning. Finally, two transient receptor potential melastatin (TRPM) channels, GON-2 and GTL-2, mediate this newly described rapid pathogen avoidance. These results suggest a mechanism by which TRPM channels may sense the intestinal distension caused by bacterial colonization to elicit pathogen avoidance and aversive learning by detecting changes in host physiology.

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Multimodal sensory processing in Caenorhabditis elegans

Cited by 42 publications

References 107 publications

Structural and developmental principles of neuropil assembly inC. elegans

Structural and developmental principles of neuropil assembly inC. elegans

Novel Technological Advances in Functional Connectomics in C. elegans

TRPM channels mediate learned pathogen avoidance following intestinal distention

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