Structural basis for degeneracy among thermosensory neurons in Caenorhabditis elegans.

Editor's Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoral fellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For more information on the format and purpose of the Journal Club, please see Review of Beverly et al. Many biological systems show degener-acy, i.e., the ability to generate the same output by multiple distinct components under varying conditions. Degeneracy contributes to robustness by imparting a certain degree of redundancy into the network. It also increases adaptability by allowing flexible recruitment of different elements in a context-dependent manner. These properties of degeneracy are well embedded in the nervous system. A single neuron can project to several downstream targets, and inputs from multiple neurons often converge on the same integration site, where the final output is modulated. This convergent– divergent feature of neu-ral connectivity provides an ideal sub-strate for functional degeneracy (Tononi et al., 1999). The nematode Caenorhabditis elegans performs a robust navigational behavior called negative thermotaxis. When placed on a thermal gradient at temperatures higher than its cultivation temperature (T C), C. elegans migrates toward colder temperatures near T C. Early studies identified ciliated AFD neurons as primary thermosensory neurons; later studies unveiled the role of AWC sensory neurons in 2008). In a recent paper published in The Journal of Neuroscience, Beverly et al. (2011) identified the ASI chemosensory neuron as a new thermosensory neuron and showed that the three sensory neuron classes act degeneratively to generate a robust negative thermotaxis. By genetic rescue and cell ablation experiments , the authors found that different combinations of AFD, AWC, and ASI neurons are sufficient or necessary for negative thermotaxis under various cultivation and assay temperatures, yet each responds to temperature stimuli uniquely in defined contexts. Particularly, ASI exhibited a stochastic Ca 2ϩ transient in response to thermal stimuli within a T C-dependent operating range, distinct from both AFD and AWC neurons. The authors suggest that the robust negative thermotactic behavior of C. elegans relies on functional degeneracy and modulation among thermosensory neurons. The novel findings emphasize that well specified conditions are essential to such quantitative analysis of animal behavior and its cellular mechanisms. An intriguing question, then, is how the newly identified ASI sensory neurons, together with other components, are engaged in a degenerate circuit underlying negative thermotaxis. One early model of thermotaxis comprises sensory …