Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Aichi, Japan.
Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo, Japan.
PLoS Comput Biol. 2021 Jan 8;17(1):e1007916. doi: 10.1371/journal.pcbi.1007916. eCollection 2021 Jan.
Motile organisms actively detect environmental signals and migrate to a preferable environment. Especially, small animals convert subtle spatial difference in sensory input into orientation behavioral output for directly steering toward a destination, but the neural mechanisms underlying steering behavior remain elusive. Here, we analyze a C. elegans thermotactic behavior in which a small number of neurons are shown to mediate steering toward a destination temperature. We construct a neuroanatomical model and use an evolutionary algorithm to find configurations of the model that reproduce empirical thermotactic behavior. We find that, in all the evolved models, steering curvature are modulated by temporally persistent thermal signals sensed beyond the time scale of sinusoidal locomotion of C. elegans. Persistent rise in temperature decreases steering curvature resulting in straight movement of model worms, whereas fall in temperature increases curvature resulting in crooked movement. This relation between temperature change and steering curvature reproduces the empirical thermotactic migration up thermal gradients and steering bias toward higher temperature. Further, spectrum decomposition of neural activities in model worms show that thermal signals are transmitted from a sensory neuron to motor neurons on the longer time scale than sinusoidal locomotion of C. elegans. Our results suggest that employments of temporally persistent sensory signals enable small animals to steer toward a destination in natural environment with variable, noisy, and subtle cues.
游动生物主动探测环境信号并迁移到更适宜的环境。特别是，小动物将感知输入中的细微空间差异转化为导向行为输出，从而直接朝着目标前进，但引导行为的神经机制仍难以捉摸。在这里，我们分析了秀丽隐杆线虫的趋热性行为，发现少量神经元介导了朝向目标温度的转向。我们构建了一个神经解剖学模型，并使用进化算法来寻找再现经验趋热行为的模型配置。我们发现，在所有进化的模型中，转向曲率是由超越秀丽隐杆线虫正弦运动时间尺度的持续时间感应热信号调制的。温度持续上升会降低转向曲率，导致模型蠕虫直线运动，而温度下降会增加曲率，导致蠕虫曲线运动。这种温度变化与转向曲率之间的关系再现了经验性的趋热迁移和朝向更高温度的转向偏差。此外，模型蠕虫中神经活动的频谱分解表明，热信号的传递时间尺度长于秀丽隐杆线虫的正弦运动，从感觉神经元传递到运动神经元。我们的结果表明，暂时持续的感觉信号的运用使小动物能够在具有可变、嘈杂和微妙线索的自然环境中朝着目标前进。
