Neural coding of thermal preferences in the nematode Caenorhabditis elegans

• Published in: eNeuro 2020-05, Vol.7 (3), p.ENEURO.0414-19.2020
• Main Authors: Matsuyama, Hironori J, Mori, Ikue
• Format: Article
• Language: English
• Subjects: New Research
• ISSN: 2373-2822; 2373-2822
• DOI: 10.1523/ENEURO.0414-19.2020

Animals are capable to modify sensory preferences according to past experiences. Surrounded by ever-changing environments, they continue assigning a hedonic value to a sensory stimulus. It remains to be elucidated however how such alteration of sensory preference is encoded in the nervous system. Here we show that past experiences alter temporal interaction between the calcium responses of sensory neurons and their postsynaptic interneurons in the nematode exhibits thermotaxis, in which its temperature preference is modified by the past feeding experience: well-fed animals are attracted toward their past cultivation temperature on a thermal gradient, whereas starved animals lose that attraction. By monitoring calcium responses simultaneously from both AFD thermosensory neurons and their postsynaptic AIY interneurons in well-fed and starved animals under time-varying thermal stimuli, we found that past feeding experiences alter phase shift between AFD and AIY calcium responses. Furthermore, the difference in neuronal activities between well-fed and starved animals observed here are able to explain the difference in the behavioral output on a thermal gradient between well-fed and starved animals. Although previous studies have shown that executes thermotaxis by regulating amplitude or frequency of the AIY response, our results proposed a new mechanism by which thermal preference is encoded by phase shift between AFD and AIY activities. Given these observations, thermal preference is likely to be computed on synapses between AFD and AIY neurons. Such a neural strategy may enable animals to enrich information processing within defined connectivity via dynamic alterations of synaptic communication. can assign a hedonic value to a temperature depending on past feeding experiences. They prefer the temperature associated with food intake, whereas lose the preference to one associated with starvation. This paradigm provides a model to elucidate how the sensory preference is encoded by the nervous system. We show here that thermal preference is encoded by temporal interaction, especially phase shift, between the responses of sensory neurons and their postsynaptic interneurons. Furthermore, the neuronal activity patterns we observed here were well correlated with behavioral outputs. Although previous studies have revealed that amplitude or frequency of interneuron responses encodes temperature information, we added a new mechanism by which phase shift between sensory