Abstract
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 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 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 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.
•The gene expression profile of AFD reflects defined temperature experience features•Altered expression is mediated by classic activity-dependent regulatory pathways•Specific gene expression changes drive developmental and behavioral flexibility•Linking stimulus aspects with transcription enables precise neuronal plasticity
Harris et al. describe how distinct features of a sensory experience are encoded in the transcriptional profile of a thermosensory neuron pair. Modification of the gene expression program via classic activity-dependent pathways drives neuronal plasticity in response to defined temperature changes and underlies concomitant behavioral adaptation.