Olfactory Behavior of Swimming C. elegans Analyzed by Measuring Motile Responses to Temporal Variations of Odorants

Abstract

Luo L, Gabel CV, Ha H-I, Zhang Y, Samuel AD. Olfactory behavior of swimming C. elegans analyzed by measuring motile responses to temporal variations of odorants. J Neurophysiol 99: 2617-2625, 2008. First published March 26, 2008 doi:10.1152/jn.00053.2008. Caenorhabditis elegans responds to chemical cues using a small number of chemosensory neurons that detect a large variety of molecules in its environment. During chemotaxis, C. elegans biases its migration in spatial chemical gradients by lengthening (/shortening) periods of forward movement when it happens to be moving toward (/away) from preferred locations. In classical assays of chemotactic behavior, a group of crawling worms is placed on an agar plate containing a point source of chemical, the group is allowed to navigate for a period of time, and aggregation of worms near the source is quantified. Here we show that swimming worms exhibit acute motile responses to temporal variations of odor in their surrounding environment, allowing our development of an automated assay of chemotactic behavior with single-animal resolution. By placing individual worms in small microdroplets and quantifying their movements as they respond to the addition and removal of odorized airstreams, we show that the sensorimotor phenotypes of swimming worms (wild-type behavior, the effects of certain mutations, and the effects of laser ablation of specific olfactory neurons) are consistent with aggregation phenotypes previously obtained in crawling assays. The microdroplet swimming assay has certain advantages over crawling assays, including flexibility and precision in defining the stimulus waveform and automated quantification of motor response during stimulus presentation. In this study, we use the microdroplet assay to quantify the temporal dynamics of the olfactory response, the sensitivity to odorant concentration, combinations, and gradients, and the contribution of specific olfactory neurons to overall behavior.

Odour concentration-dependent olfactory preference change in C. elegans

“…1c). These results indicate that the odorant preference of C. elegans alters depending on the concentration of various odorants, consistent with the previous reports that high concentrations of several odorants caused avoidance behaviour 8,11,12 . Because of the abundant knowledge about isoamyl alcohol based on laser ablation experiments, calcium imaging experiments and others, we focused on isoamyl alcohol in this study 8,13 .…”

“…ODR-3 was previously reported to be expressed in five pairs of sensory neurons, AWA, AWB, AWC, ASH and ADF 20 . Among these neurons, AWB and ASH sensory neurons are known to mediate avoidance of volatile odorants [9][10][11][12] . Avoidance defects of the odr-3 mutants were rescued by either AWB-or ASH-specific expression of odr-3 cDNA (Fig.…”

Parallel Use of Two Behavioral Mechanisms for Chemotaxis inCaenorhabditis elegans

“…It was recently demonstrated that C. elegans also respond to a decrease in the concentration of odorants by increasing the frequency of reversals (Chalasani et al, 2007;Luo et al, 2008). These observations are consistent with the assumption that odorant chemotaxis is also achieved by the pirouette strategy.…”

“…In fact, in addition to the result of tracking analyses (PierceShimomura et al, 1999), various behavioral analyses have supported this model: by using glued animals and semirestrained animals, it was shown that worms show a reversal response to a decrease in salt concentration (Dusenbery, 1980;Miller et al, 2005). Similar reversal responses were detected for odorants (Chalasani et al, 2007;Luo et al, 2008). Behavioral analyses of the temperature response also supported the pirouette model (Ryu and Samuel, 2002).…”

Dissecting a central flip-flop circuit that integrates contradictory sensory cues in C. elegans feeding regulation

“…1d), a defect which was fully rescued by introducing the odr-10 and odr-7 genomic transgenes, respectively (Supplementary Figs S3,S4). The ceh-36 gene is required for the development and function of AWC neurons 10,11 , while the odr-10 gene is normally expressed exclusively in AWA neurons under the control of odr-7 and encodes a G-protein-coupled receptor that detects diacetyl [7][8] . These data indicate that diacetyl induces feeding facilitation mainly via sensing through the AWA sensory neurons.…”