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 ...

A memory of prior thermal experience governs Caenorhabditis elegans thermotactic behavior. On a spatial thermal gradient, C. elegans tracks isotherms near a remembered temperature we call the thermotactic set-point (T(S)). The T(S) corresponds to the previous cultivation temperature and can be reset by sustained exposure to a new temperature. The mechanisms underlying this behavioral plasticity are unknown, partly because sensory and experience-dependent components of thermotactic behavior have been difficult to separate. Using newly developed quantitative behavioral analyses, we demonstrate that the T(S) represents a weighted average of a worm's temperature history. We identify the DGK-3 diacylglycerol kinase as a thermal memory molecule that regulates the rate of T(S) resetting by modulating the temperature range of synaptic output, but not temperature sensitivity, of the AFD thermosensory neurons. These results provide the first mechanistic insight into the basis of experience-dependent plasticity in this complex behavior.

Transcriptional profiling experiments identify light- and temperature-entrained circadian transcripts in C. elegans.

SUMMARY Background The neuronal mechanisms that encode specific stimulus features in order to elicit defined behavioral responses are poorly understood. C. elegans forms a memory of its cultivation temperature (Tc) and exhibits distinct behaviors in different temperature ranges relative to Tc. In particular, C. elegans tracks isotherms only in a narrow temperature band near Tc. Tc memory is in part encoded by the threshold of responsiveness (T*AFD) of the AFD thermosensory neuron pair to temperature stimuli. However, since AFD thermosensory responses appear to be similar at all examined temperatures above T*AFD, the mechanisms that generate specific behaviors in defined temperature ranges remain to be determined. Results Here, we show that the AFD neurons respond to the sinusoidal variations in thermal stimuli followed by animals during isothermal tracking (IT) behavior only in a narrow temperature range near Tc. We find that mutations in the AFD-expressed gcy-8 receptor guanylyl cyclase (rGC) gene result in defects in the execution of IT behavior, and are associated with defects in the responses of the AFD neurons to oscillating thermal stimuli. In contrast, mutations in the gcy-18 or gcy-23 rGCs alter the temperature range in which IT behavior is exhibited. Alteration of intracellular cGMP levels via rGC mutations or addition of cGMP analogs shift the lower and upper ranges of the temperature range of IT behavior in part via alteration in T*AFD. Conclusions Our observations provide insights into the mechanisms by which a single sensory neuron type encodes features of a given stimulus to generate different behaviors in defined zones.

Carbon dioxide (CO(2)) elicits an attractive host-seeking response from mosquitos yet is innately aversive to Drosophila melanogaster despite being a plentiful byproduct of attractive fermenting food sources. Prior studies used walking flies exclusively, yet adults track distant food sources on the wing. Here we show that a fly tethered within a magnetic field allowing free rotation about the yaw axis actively seeks a narrow CO(2) plume during flight. Genetic disruption of the canonical CO(2)-sensing olfactory neurons does not alter in-flight attraction to CO(2); however, antennal ablation and genetic disruption of the Ir64a acid sensor do. Surprisingly, mutation of the obligate olfactory coreceptor (Orco) does not abolish CO(2) aversion during walking yet eliminates CO(2) tracking in flight. The biogenic amine octopamine regulates critical physiological processes during flight, and blocking synaptic output from octopamine neurons inverts the valence assigned to CO(2) and elicits an aversive response in flight. Combined, our results suggest that a novel Orco-mediated olfactory pathway that gains sensitivity to CO(2) in flight via changes in octopamine levels, along with Ir64a, quickly switches the valence of a key environmental stimulus in a behavioral-state-dependent manner.