Hierarchical sparse coding in the sensory system of Caenorhabditis elegans

Significance We investigated how a numerically and spatially compact nematode nervous system encodes information about the world. A library of transgenic worms expressing a genetically encoded calcium indicator in each type of sensory neuron was constructed and used to assay neural activity in response to various chemical stimuli to compile a functional map of a sensory system. We find that the sensory system uses hierarchical sparse coding, a strategy that mitigates the limited size and the shallow structure of the neural network. Also, this is a timely study that significantly adds to the communal effort and enthusiasm in obtaining functional maps of the connectome. Animals with compact sensory systems face an encoding problem where a small number of sensory neurons are required to encode information about its surrounding complex environment. Using Caenorhabditis elegans worms as a model, we ask how chemical stimuli are encoded by a small and highly connected sensory system. We first generated a comprehensive library of transgenic worms where each animal expresses a genetically encoded calcium indicator in individual sensory neurons. This library includes the vast majority of the sensory system in C. elegans. Imaging from individual sensory neurons while subjecting the worms to various stimuli allowed us to compile a comprehensive functional map of the sensory system at single neuron resolution. The functional map reveals that despite the dense wiring, chemosensory neurons represent the environment using sparse codes. Moreover, although anatomically closely connected, chemo- and mechano-sensory neurons are functionally segregated. In addition, the code is hierarchical, where few neurons participate in encoding multiple cues, whereas other sensory neurons are stimulus specific. This encoding strategy may have evolved to mitigate the constraints of a compact sensory system.