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Behavioral strategy of chemotaxis
Have you ever found yourself tempted by delicious smell and walking unintentionally to a restaurant? Taxis refers to the oriented movement of an organism in response to external stimulus such as odor, light, temperature, magnetic field, etc. Taxis is seen in many organisms. For example the phrase “a moth flying into the flame” refers to the habit of insects moving toward light. Even unicellular organism like E. coli shows taxis to chemicals, known as chemotaxis. C. elegans also shows taxis like chemotaxis and thermotaxis, but in fact there are two different mechanisms that generate taxis.
The first one is pirouette mechanism in which the worms change their frequency of turning at an acute angle. Cultured under high NaCl concentration, worms become attracted to NaCl. In this case the turning frequency increases when the NaCl concentration decrease. The worms remember that there was food where NaCl concentration was high. Therefore decrease of NaCl appears to them as if they are going away from the food. On the contrary, increase of NaCl concentration during forward movement appears as if they are getting nearer to the food. This reduces the turning frequency and the worms continue moving forward. This turning behavior is called pirouette behavior, and pirouette mechanism refers to the behavioral strategy in which the worms aim for their ideal environment by regulating the frequency of pirouette behavior. Pirouette mechanism in C. elegans was found by Pierce-Shimomura and his group in 1999. As a similar mechanism, “biased random walk” in E. coli (commentary) is known.
The second mechanism is called weathervane mechanism. In this mechanism the worms compare the chemical concentration of their ventral side with that of dorsal side and curve gently to the preferable side (note that C. elegans usually lies on its side on a flat surface). In particular, if C. elegans were cultured on a high NaCl concentration, they tend to curve gently to high NaCl on a NaCl gradient plate. It was difficult to prove the existence of weathervane mechanism because pirouette occurs if the NaCl concentration change is drastic. But in 2009 our careful observation revealed the existence of weathervane mechanism and identified some pairs of neurons required for these mechanisms3.
These mechanisms in chemotaxis were investigated with the help of video tracking system. This system can recognize C. elegans automatically and record the trajectories of their movement. The collected data was analyzed by computer.
＜reference：description of the system used in Iino and Yoshida., 2009＞
Movie1 Pirouette behavior: The worm bends its body and changes its orientation after a reversal. Figure1 NaCl chemotaxis behavior using pirouette mechanism and weathervane mechanism: black line shows the trajectory and orientation of the worm, blue shows the gradient of NaCl concentration.
By investigating not only behaviors but also the strategies regulating those behaviors may lead us to understand how the neural circuit works.
To reveal the mechanism of neural circuit, we are taking several approaches. Recently we can manipulate the neural circuit artificially by ablating specific neurons by laser or activating specific neurons by optogenetics. We can also observe neural activity by calcium imaging.
1. Pierce-Shimomura et al., The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci. 1999 Nov 1;19(21):9557-69.
2. Macbab et al., The Gradient-Sensing Mechanism in Bacterial Chemotaxis. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2509-12.
3. Iino and Yoshida, Parallel Use of Two Behavioral Mechanisms for Chemotaxis in Caenorhabditis elegans. J Neurosci. 2009 Apr 29;29(17):5370-80.
4. Satoh et al, Regulation of Experience-Dependent Bidirectional Chemotaxis by a Neural Circuit Switch in Caenorhabditis elegans. J Neurosci. 2014 Nov 19;34(47):15631-7.