Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

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Abstract:

The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (Ts) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above Ts (negative thermotaxis) and performs isothermal tracking near Ts. Under some conditions, the worm migrates up temperature gradients below Ts (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward Ts to study the role of specific neurons that have been proposed to be involved in thermotaxis using genetic ablation, behavioral tracking, and calcium imaging. We find differences in the strategies for positive and negative thermotaxis. Negative thermotaxis is achieved through biasing the frequency of reorientation maneuvers (turns and reversal turns) and biasing the direction of reorientation maneuvers toward colder temperatures. Positive thermotaxis, in contrast, biases only the direction of reorientation maneuvers toward warmer temperatures. We find that the AFD thermosensory neuron drives both positive and negative thermotaxis. The AIY interneuron, which is postsynaptic to AFD, may mediate the switch from negative to positive thermotaxis below Ts. We propose that multiple thermotactic behaviors, each defined by a distinct set of sensorimotor transformations, emanate from the AFD thermosensory neurons. AFD learns and stores the memory of preferred temperatures, detects temperature gradients, and drives the appropriate thermotactic behavior in each temperature regime by the flexible use of downstream circuits.

Notes:

Luo, LinjiaoCook, NathanVenkatachalam, VivekMartinez-Velazquez, Luis AZhang, XiaodongCalvo, Ana CHawk, JoshMacInnis, Bronwyn LFrank, MichelleNg, Jia Hong RayKlein, MasonGershow, MarcHammarlund, MarcGoodman, Miriam BColon-Ramos, Daniel AZhang, YunSamuel, Aravinthan D Teng1P01GM103770/GM/NIGMS NIH HHS/8DP1GM105383-05/DP/NCCDPHP CDC HHS/P01 GM103770/GM/NIGMS NIH HHS/R01 DC009852/DC/NIDCD NIH HHS/R01 NS076558/NS/NINDS NIH HHS/R01NS076558/NS/NINDS NIH HHS/R21 NS061147/NS/NINDS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov'tResearch Support, U.S. Gov't, Non-P.H.S.2014/02/20 06:00Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2776-81. doi: 10.1073/pnas.1315205111. Epub 2014 Feb 3.