OLA-1, an Obg-like ATPase, integrates hunger with temperature information in sensory neurons in C. elegans

Abstract

Animals detect changes in both their environment and their internal state and modify their behavior accordingly. Yet, it remains largely to be clarified how information of environment and internal state is integrated and how such integrated information modifies behavior. Well-fed C. elegans migrates to past cultivation temperature on a thermal gradient, which is disrupted when animals are starved. We recently reported that the neuronal activities synchronize between a thermosensory neuron AFD and an interneuron AIY, which is directly downstream of AFD, in well-fed animals, while this synchrony is disrupted in starved animals. However, it remained to be determined whether the disruption of the synchrony is derived from modulation of the transmitter release from AFD or from the modification of reception or signal transduction in AIY. By performing forward genetics on a transition of thermotaxis behavior along starvation, we revealed that OLA-1, an Obg-like ATPase, functions in AFD to promote disruption of AFD-AIY synchrony and behavioral transition. Our results suggest that the information of hunger is delivered to the AFD thermosensory neuron and gates transmitter release from AFD to disrupt thermotaxis, thereby shedding light onto a mechanism for the integration of environmental and internal state to modulate behavior. Author summary As we humans perceive food smell more attractive when we are hungry, animal’s internal state such as satiety affects their sensory stimulus-induced behavior. However, it is not fully understood how multiple external and internal inputs are integrated in the nervous system to modify behavior. In this study, we analyzed the effect of starvation on the thermotaxis behavior of the nematode C. elegans. Animals migrate toward past cultivation temperature on a thermal gradient without food, which is disrupted by starvation. We have found that an ATPase, called OLA-1, which is universally conserved both in prokaryotes and eukaryotes, acts in the thermosensory neuron to modulate its communication with a downstream interneuron, resulting in a modification of the thermotaxis behavior. Our results provided a molecular and neural-circuit mechanism by which animals integrate information of their internal state with that of the external environment to modify their behavior.