The molecular and physiological basis of thermosensory behaviors in Caenorhabditis elegans

Organisms utilize a variety of senses to judge the nature of their environment. External sensory cues influence internal state, resulting in altered behavioral output. Here we examine the molecules and circuits mediating thermotactic navigation behavior in the nematode Caenorhabditis elegans. C. elegans senses its cultivation temperature and creates a 'memory' of this temperature, which in turn dictates its navigation behavioral strategy, as can be seen on a spatial or temporal thermal gradient. At temperatures greater than its cultivation temperature, C. elegans moves down the gradient toward cooler temperatures, whereas in a 2ºC band around its cultivation temperature, C. elegans tracks isotherms. The ability to track isotherms on spatial gradients requires that animals be able to sense rapid rates of temperature change and modulate their locomotor behavior accordingly. The AFD thermosensory neurons are the major mediators of temperature-dependent navigation behaviors. This neuron type has been reported to be extraordinarily thermosensitive, and is able to respond to temperature differences of as little as 0.003ºC. The molecular basis of this thermosensitivity is unclear. I show that the GCY-8, GCY-18 and GCY-23 receptor guanylyl cyclases play roles in conferring the extraordinary temperature sensitivity of the AFD neurons. These three molecules are required for AFD-mediated isothermal tracking behavior, and also regulate the setting of cultivation temperature memory in the AFD neurons. While the AFD thermosensory neurons are likely instructive for the generation of isothermal tracking behavior, I find that the AWC olfactory neurons are also thermosensitive, and play a permissive role in the execution of isothermal tracking behavior. Analysis of the molecular and neuronal basis of thermosensory behaviors in C. elegans may provide insight into the mechanisms by which animals sense and respond to complex environmental cues.