Neural signal propagation atlas of C. elegans

TL;DR

This study maps functional neural signal propagation in C. elegans, revealing that extrasynaptic signaling significantly influences neural dynamics beyond anatomical predictions, emphasizing the importance of functional measurements.

Contribution

The paper provides the first comprehensive functional atlas of neural signal propagation in C. elegans, highlighting the role of extrasynaptic signaling in neural function.

Findings

Signal propagation differs from anatomical predictions.

Extrasynaptic signaling contributes significantly to neural activity.

Functional propagation better predicts neural dynamics than anatomy.

Abstract

A fundamental problem in neuroscience is understanding how a network's properties dictate its function. Connectomics provides one avenue to predict nervous system function. To test this explicitly, we systematically measure signal propagation in 23,427 pairs of neurons across the head of the nematode Caenorhabditis elegans by direct optogenetic activation and simultaneous whole-brain calcium imaging. We measure the sign (excitatory or inhibitory), strength, temporal properties, and causal direction of signal propagation between these neurons to create a functional atlas. We find that signal propagation differs from predictions based on anatomy. Using mutants, we show that extrasynaptic signaling not visible from anatomy contributes to this difference. We identify many instances of dense-core-vesicle dependent signaling on seconds-or-less timescales that evoke acute calcium transients often where no direct wired connection exists but where relevant neuropeptides and receptors are expressed. We propose that here extrasynaptically released neuropeptides serve a similar function as that of classical neurotransmitters. Finally, our measured signal propagation atlas better predicts neural dynamics of spontaneous activity than does anatomy. We conclude that both synaptic and extrasynaptic signaling drive neural dynamics on short timescales and that measurement of evoked signal propagation are critical for interpreting neural function.