Multiparameter behavioral profiling reveals distinct thermal response regimes in Caenorhabditis elegans
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RESEARCH ARTICLE
Open Access
Multiparameter behavioral profiling reveals distinct thermal response regimes in Caenorhabditis elegans Rajarshi Ghosh1, Aylia Mohammadi2, Leonid Kruglyak1,3 and William S Ryu2,4*
Abstract Background: Responding to noxious stimuli by invoking an appropriate escape response is critical for survival of an organism. The sensations of small and large changes in temperature in most organisms have been studied separately in the context of thermotaxis and nociception, respectively. Here we use the nematode C. elegans to address the neurogenetic basis of responses to thermal stimuli over a broad range of intensities. Results: C. elegans responds to aversive temperature by eliciting a stereotypical behavioral sequence. Upon sensation of the noxious stimulus, it moves backwards, turns and resumes forward movement in a new direction. In order to study the response of C. elegans to a broad range of noxious thermal stimuli, we developed a novel assay that allows simultaneous characterization of multiple aspects of escape behavior elicited by thermal pulses of increasing amplitudes. We exposed the laboratory strain N2, as well as 47 strains with defects in various aspects of nervous system function, to thermal pulses ranging from ΔT = 0.4°C to 9.1°C and recorded the resulting behavioral profiles. Conclusions: Through analysis of the multidimensional behavioral profiles, we found that the combinations of molecules shaping avoidance responses to a given thermal pulse are unique. At different intensities of aversive thermal stimuli, these distinct combinations of molecules converge onto qualitatively similar stereotyped behavioral sequences. Keywords: Nociception, dimensionality reduction, ethology, thermal sensation
Background An organism’s environment is characterized by temporal and spatial fluctuations of temperature. The ability of the nervous system to elicit appropriate behavioral responses to a range of thermal stimuli is critical for the animal’s survival. At the molecular level, the perception of different temperature ranges, at least in mammals, is determined by the activation thresholds of relevant neurons set by distinct combinations of transient receptor potential (TRP) and potassium channels [1,2]. However, beyond these thermosensors, the behavioral, neural and molecular correlates of the transformation of temperature perception to behavioral outputs are less well understood. * Correspondence: [email protected] 2 Department of Physics, University of Toronto, St George Street, Toronto, Canada Full list of author information is available at the end of the article
The nematode C. elegans is an ideal model system for uncovering the molecular and cellular bases of perception of a variety of thermal stimuli [3-5]. Depending on the nature of the thermal stimulus, C. elegans displays distinct behaviors. During thermotaxis it can discriminate temperature differences of approximately 0.05°C [6]. At the other extreme, temperatures approximately 16°C above the baseline elicit a stereotypi
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