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

Neurons modify their molecular profiles 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 temperature 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, and 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 elements 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. Overall design: Differential gene expression from C. elegans AFD neurons in worms that have experienced 15 vs 25 degrees celsius. AFD-specific mRNA isolated using Translating Ribosome Affinity Purification (AFD_15 and AFD_25 samples). RNA from whole animal lysates was also sequenced for comparison (whole_15 and whole_25 samples).