Neuron ID dataset facilitates neuronal annotation for whole-brain activity imaging of C. elegans

Abstract

Background: Annotation of cell identity is an essential process in neuroscience that allows comparison of cells, including that of neural activities across different animals. In Caenorhabditis elegans, although unique identities have been assigned to all neurons, the number of annotatable neurons in an intact animal has been limited due to the lack of quantitative information on the location and identity of neurons.Results: Here, we present a dataset that facilitates the annotation of neuronal identities, and demonstrate its application in a comprehensive analysis of whole-brain imaging. We systematically identified neurons in the head region of 311 adult worms using 35 cell-specific promoters and created a dataset of the expression patterns and the positions of the neurons. We found large positional variations that illustrated the difficulty of the annotation task. We investigated multiple combinations of cell-specific promoters driving distinct fluorescence and generated optimal strains for the annotation of most head neurons in an animal. We also developed an automatic annotation method with human interaction functionality that facilitates annotations needed for whole-brain imaging. Conclusion: Our neuron ID dataset and optimal fluorescent strains enable the annotation of most neurons in the head region of adult C. elegans, both in full-automated fashion and a semi-automated version that includes human interaction functionalities. Our method can potentially be applied to model species used in research other than C. elegans, where the number of available cell-type-specific promoters and their variety will be an important consideration.

Principles for coding associative memories in a compact neural network

“…Whole-brain functional imaging enables measuring activity from large volumes in animals that express activity-dependent fluorescent markers (Ahrens et al , 2013;Aimon et al , 2019;Voleti et al , 2019) . In C. elegans , advanced microscopy techniques allow imaging neural dynamics of the entire network with cellular resolution in both stationary and freely-behaving animals (Schrödel et al , 2013;Kato et al , 2015;Nguyen et al , 2016;Venkatachalam et al , 2016;Toyoshima et al , 2020) .…”

Toward a More Accurate 3D Atlas ofC. elegansNeurons

“…A complicating factor in position-derived identification is that individual neuron positions are known to be locally variable between different worms ( Wall et al, 2007; Toyoshima et al, 2020; Yemini et al, 2021 ). This is caused partly by C. elegans size and shape differences, and partly because of inherent positional variance that may be so extreme as to have nearby neurons switch relative positions.…”

“…This illustrative 1986 worm atlas has often been treated as canon, or at least as an atlas of sufficient quality to compare with contemporary data from modern and more reproducible measurement techniques. This is in large part due to it being the only atlas of its kind up until very recently ( Toyoshima et al, 2020; Yemini et al, 2021 ). For example, Scholz et al .…”

“…OpenWorm presents information for individual neurons and their connectivity, assembled into a 3D approximation of an adult hermaphrodite worm. However, the inherent positional variability of neurons in the head and tail is now readily apparent from multicolor C. elegans strains, designed for neural identification, that were used to measure neuron positions and their variability across multiple animals ( Toyoshima et al, 2020; Varol et al, 2020; Yemini et al, 2021 ). These strains and concurrent algorithmic advances demonstrate how fluorescent-protein barcodes can be used to accurately determine neuron identities in volumetric images ( Bubnis et al, 2019; Nejatbakhsh et al, 2020; Mena et al, 2020; Chaudhary et al, 2021; Yu et al, 2021; Wen et al, 2021 ).…”

Wired for insight—recent advances in Caenorhabditis elegans neural circuits

“…In fact, positions of neurons in the ganglia of adult animals are quite variable. For example, a comprehensive analysis of 311 adults using 35 fluorescence reporters for neurons in the head reported large positional variations, posing caveats for position-based cell annotation (TOYOSHIMA et al 2020). Now, a new approach called Neuronal Polychromatic Atlas of Landmarks (NeuroPAL) enables simultaneous identification of neurons in the entire nervous system (YEMINI et al 2021) (Table 1).…”