Molecular encoding of stimulus features in a single sensory neuron type enables neuronal and behavioral plasticity

Neurons modify their transcriptomes in response to an animal's experience. How specific experiences are transduced to modulate gene expression and precisely tune neuronal functions are not fully defined. Here, we describe the molecular profile of a thermosensory neuron pair in C. elegans experiencing different tem-perature stimuli. We find that distinct salient features of the temperature stimulus, including its duration, magnitude of change, and absolute value, are encoded in the gene expression program in this single neuron type, and we identify a novel transmembrane protein and a transcription factor whose specific transcriptional dynamics are essential to drive neuronal, behavioral, and developmental plasticity. Expression changes are driven by broadly expressed activity-dependent transcription factors and corresponding cis-regulatory ele-ments that nevertheless direct neuron-and stimulus-specific gene expression programs. Our results indicate that coupling of defined stimulus characteristics to the gene regulatory logic in individual specialized neuron types can customize neuronal properties to drive precise behavioral adaptation.

Automated summary

Neurons modify their transcriptomes in response to an animal's experience, and specific experiences transduce to modulate gene expression and precisely tune neuronal functions. In this study, the molecular profile of a thermosensory neuron pair in C. elegans experiencing different temperature stimuli is described. The results reveal that distinct features of the temperature stimulus are encoded in the gene expression program in this single neuron type, and specific transcriptional dynamics of certain genes are essential for neuronal, behavioral, and developmental plasticity.