The thermotactic behaviors of Caenorhabditis elegans indicate that its thermosensory system exhibits exquisite temperature sensitivity, long-term plasticity, and the ability to transform thermosensory input into different patterns of motor output. Here, we study the physiological role of the AFD thermosensory neurons by quantifying intracellular calcium dynamics in response to defined temperature stimuli. We demonstrate that short-term adaptation allows AFD to sense temperature changes as small as 0.05°C over temperature ranges as wide as 10°C. We show that a bidirectional thermosensory response (increasing temperature raises and decreasing temperature lowers the level of intracellular calcium in AFD) allows the AFD neurons to phase-lock their calcium dynamics to oscillatory thermosensory inputs. By analyzing the thermosensory response of AFD dendrites severed from their cell bodies by femtosecond laser ablation, we show that long-term plasticity is encoded as shifts in the operating range of a putative thermoreceptor(s) in the AFD sensory endings. Finally, we demonstrate that AFD activity is directly coupled to stimulation of its postsynaptic partner AIY. These observations indicate that many functions underlying thermotactic behavior are properties of one sensory neuronal type. Encoding multiple functions in individual sensory neurons may enable C. elegans to perform complex behaviors with simple neuronal circuits.

Iwanir S; Tramm N; Nagy S; Wright C; Ish D; Biron D. The microarchitecture of C. elegans behavior during lethargus: homeostatic bout dynamics, a typical body posture, and regulation by a central neuron. SLEEP 2013;36(3):385-395.

Caenorhabditis elegans navigates thermal gradients by using a behavioral strategy that is regulated by a memory of its cultivation temperature (Tc). At temperatures above or around the Tc, animals respond to temperature changes by modulating the rate of stochastic reorientation events. The bilateral AFD neurons have been implicated as thermosensory neurons, but additional thermosensory neurons are also predicted to play a role in regulating thermotactic behaviors. Here, we show that the AWC olfactory neurons respond to temperature. Unlike AFD neurons, which respond to thermal stimuli with continuous, graded calcium signals, AWC neurons exhibit stochastic calcium events whose frequency is stimulus-correlated in a T c-dependent manner. Animals lacking the AWC neurons or with hyperactive AWC neurons exhibit defects in the regulation of reorientation rate in thermotactic behavior. Our observations suggest that the AFD and AWC neurons encode thermal stimuli via distinct strategies to regulate C. elegans thermotactic behavior.calcium imaging ͉ G protein-coupled receptor ͉ AWC neuron ͉ isothermal tracking M any animals navigate their environment by using behavioral strategies that are probabilistic in nature. In the biased random-walk strategy used by Escherichia coli and Caenorhabditis elegans to navigate chemical gradients, periods of forward movement are interrupted by turns or reversals that reorient the organism (1, 2). The frequency of reorientation events is governed by environmental cues and the animal's past experience, but the occurrence of individual turns and reversals is unpredictable and stochastic (3-6). The mechanisms by which sensory neurons and downstream circuits modulate the probability of reorientation events in complex organisms is not well understood.C. elegans thermotactic behavior provides an excellent system in which to explore the sensorimotor strategies underlying behavior. The behavior of C. elegans on a thermal gradient depends on a memory of its cultivation temperature (T c ) (7). At temperatures (T) that are higher than the T c (TϾT c ), animals move down the gradient (cryophilic behavior). Cryophilic behavior is mediated by a biased random-walk strategy such that animals decrease turning frequency when moving down the gradient and increase turning frequency when moving up the gradient (8). At TϳT c , animals exhibit a distinct behavior called isothermal tracking, where they orient perpendicular to the gradient and follow isotherms by suppressing turns (7). Thus, regulation of turning rate is critical for C. elegans thermotactic behavior.Components of the neuronal circuit underlying thermotactic behaviors in C. elegans have been identified (9). The bilateral AFD thermosensory neurons are major thermosensory neurons in the circuit (9). The AFD neurons respond to temperature stimuli only above a threshold temperature corresponding to the T c , thereby providing a cellular correlate for the T c memory (10-12). However, the AFD neurons are similarly active in the temperature ranges at which ...