The ability to achieve homeostasis in the face of varying environmental conditions is vitally important to the survival of an organism. A critical aspect of homeostasis is maintaining a temperature suitable for cellular processes. Using the model C. elegans, the Sengupta lab examined the neural circuits underlying their major thermoregulation strategy, negative thermotaxis (moving away from high temperatures). C. elegans accomplish this task using a biased random walk strategy, where the organism makes random turns and walks for longer distances when moving towards favorable temperatures and shorter distances when moving towards unfavorable temperatures.
Multiple thermosensory neuron types, including AFD and AWC neurons, contribute in producing negative thermotaxis. The authors label ASI neurons as part of the thermoregulatory circuit and give evidence supporting the notion that these different neuron types can act degenerately. By degenerately it is meant that multiple components can work under varying contexts to generate output, producing flexibility impossible with a single dedicated network that only works under certain conditions.
AFD, AWC, and ASI neurons generate temperature-evoked activity. The neurons respond to a temperature range based off the organism’s cultivation temperature (Tc). The authors establish that the different neuron types can promote negative thermotaxis under different specific conditions. Ablating only one of the neuron types at a time abolishes negative thermotaxis in only a subset of conditions. Together, the multiple systems create flexibility to robustly perform this strategy at varying conditions, each type operating in unique ways to accomplish a vital function for survival.
Above: Diagram of the experimental environment with a gradient of warmer to cooler temperatures. Wild type worms display increasing negative thermotaxis (walking towards cooler temperatures with greater bias) at increasing temperatures relative to their cultivation temperature. Negative thermotaxis declines at temperatures far from Tc when Tc = 15°C (B) but not when Tc = 20°C (C) (perhaps because of compensatory input from nociceptive circuits). The Tax-4 channel is important for thermotactic behaviors and expressed in AFD and AWC neurons. Tax-4 mutants do not produce negative thermotaxis at any experimental condition (B and C). Tax-4 is necessary for negative thermotaxis.
When certain neuron types are ablated, worms display deficiencies in negative thermotaxis in a context-dependent manner. Ablation of one chemosensory neuron type leads to different deficiencies than ablation of a different neuron type (A – E above). Ablation of AFD neurons destroys negative thermotaxis whenTc = 15°C and worms placed at a temperature 6°C above Tc. Behavior can be restored by expressing pkc-1(gf) (which drives cellular activity) in ASI and AWC neurons (F). This is part of the evidence that suggests that multiple systems act degenerately to produce negative thermotaxis.
The above data is a small subset of that contained in the Beverly et al. 2011 paper. For further discussion of the discoveries from the Sengupta lab, please join us on Tuesday, December 11th at 4 pm in Leichtag 107 (note location change!) for Piali Sengupta’s talk, titled “Running hot and cold: Robustness and flexibility in a small thermosensory circuit in C. elegans”.
The lab of Dr. Sengupta uses molecular genetic approaches in C. elegans to research the circuits and signaling pathways that allow organisms to respond to environmental cues.
H. Sequoyah Reynoso is a first year in the neurosciences Ph.D. program. He’s completing his first rotation in the lab of Dr. Adam Aron.
Beverly M., Anbil S. & Sengupta P. (2011). Degeneracy and Neuromodulation among Thermosensory Neurons Contribute to Robust Thermosensory Behaviors in Caenorhabditis elegans, Journal of Neuroscience, 31 (32) 11718-11727. DOI: 10.1523/JNEUROSCI.1098-11.2011