How many neurons does it take to stay cool?

The worm (nematode) C. elegans is a nice model system for studying neuroscience, combining

• genetic tools that allow genes to be turned on or off, often on a per cell basis, in the whole organism,
• tools like laser or genetic ablation that allow individual, identified cells to be selectively eliminated,
• robust behaviors that can be readily measured, and
• a well defined nervous system consisting of 302 neurons, each of which can be identified, and whoseanatomical connectivity has been established.

In a paper appearing this month in Journal of Neuroscience, Molecular and Cell Biology grad student Matthew Beverly, undergrad Sriram Anbil, and Professor of Biology Piali Sengupta examined the contribution of sensory neurons to controlling thermotaxis in C. elegans. Worms develop a memory of the temperature at which they have been cultivated, and display a robust behavior in which worms placed on a temperature gradient at temperatures higher than their cultivation temperature will crawl back towards colder temperature (negative thermotaxis – see movie). The behavior depends on TAX-4, a channel protein expressed in a subset of the sensory neurons. In this study, the Brandeis researchers asked the question “how many and which of the sensory neurons are required for the worms to perform negative thermotaxis, and are the required sensory neurons the same regardless of the temperature range examined?” (or, in my paraphrase, “how many and which neurons does it take to stay cool?”)

Worm head, showing expression of the calcim indicator GCaMP in ASI and AWA neurons (used in calcium imaging experiments)

As it turns out, the answer is complicated (and readers are encouraged to read the paper). The researchers found that in addition to the previously known thermosensory neurons AFD and AWC, the ASI neurons previously known to be involved in chemosensation play a significant role in regulating negative thermotaxis. Interestingly, the circuits used seem to be degenerate; under one condition, for example, a particular combination of AFD, AWC or ASI is necessary to generate the behavior, although at other conditions, a different combination is required to generate the same behavior.. And only a couple of degrees Celsius makes a difference — the circuit required for negative thermotaxis on a gradient centered at 8^oC above the cultivation temperature is different from a gradient centered at 6^oC above.

These and other results taken together suggest that even in the worm, a complex circuit has evolved to control crawling behaviors to cope with temperature changes, and that having degeneracy in the underlying circuits may be a common feature that ensures that behaviors crucial to survival are maintained in a variety of environmental conditions..

Beverly M, Anbil S, Sengupta P. Degeneracy and Neuromodulation among Thermosensory Neurons Contribute to Robust Thermosensory Behaviors in Caenorhabditis elegans. J Neurosci. 2011;31(32):11718-27.