Age‐dependent changes in response property and morphology of a thermosensory neuron and thermotaxis behavior in Caenorhabditis elegans

Age‐dependent cognitive and behavioral deterioration may arise from defects in different components of the nervous system, including those of neurons, synapses, glial cells, or a combination of them. We find that AFD, the primary thermosensory neuron of Caenorhabditis elegans , in aged animals is characterized by loss of sensory ending integrity, including reduced actin‐based microvilli abundance and aggregation of thermosensory guanylyl cyclases. At the functional level, AFD neurons in aged animals are hypersensitive to high temperatures and show sustained sensory‐evoked calcium dynamics, resulting in a prolonged operating range. At the behavioral level, senescent animals display cryophilic behaviors that remain plastic to acute temperature changes. Excessive cyclase activity of the AFD‐specific guanylyl cyclase, GCY‐8, is associated with developmental defects in AFD sensory ending and cryophilic behavior. Surprisingly, loss of the GCY‐8 cyclase domain reduces these age‐dependent morphological and behavioral changes, while a prolonged AFD operating range still exists in gcy‐8 animals. The lack of apparent correlation between age‐dependent changes in the morphology or stimuli‐evoked response properties of primary sensory neurons and those in related behaviors highlights the importance of quantitative analyses of aging features when interpreting age‐related changes at structural and functional levels. Our work identifies aging hallmarks in AFD receptive ending, temperature‐evoked AFD responses, and experience‐based thermotaxis behavior, which serve as a foundation to further elucidate the neural basis of cognitive aging.