A framework for analyzing global Caenorhabditis elegans neural activity.

Abstract

Neurons represent changes in external and internal environments by altering their activity patterns. While coherent brain-wide patterns of neural activity have been observed in neuronal populations, very little is known about their dimensionality, geometry, and how they are correlated with sensory inputs. Here, we recorded the activity of most head neurons in Caenorhabditis elegans experiencing changes in bacterial or control buffer stimuli around their nose. We first classified active neurons into six functional clusters: two sensory neuron clusters (ON and OFF responding to addition and removal of stimuli, respectively) and four motor/command neuron clusters (AVA, RME, SMDD, and SMDV). Next, we estimated stimulus selectivity for each cluster and found that while sensory neurons exhibit their maximal responses within 15 s, changes in bacterial stimuli drive maximal responses in command and motor neuron clusters after tens of seconds. Furthermore, we show that bacterial stimuli induce neural dynamics that are best described by a hyperbolic, not Euclidean, space indicating hierarchical organization in C. elegans neural population dynamics. This space was 8-dimensional, with dimensions that aligned in one sensory direction (ON and OFF neurons), two motor directions (forward-backward and dorsal-ventral), and the rest of dimensions corresponding with unclassified neurons. Collectively, we show that C. elegans neural activity can be effectively represented in low-dimensional hyperbolic space and describe how sensory information is processed by the neural network.