Data from: Habituation in non-neural organisms: evidence from slime moulds

Learning, defined as a change in behaviour evoked by experience, has hitherto been investigated almost exclusively in multicellular neural organisms. Evidence for learning in non-neural multicellular organisms is scant and only a few unequivocal reports of learning have been described in single celled organisms. Here we demonstrate habituation, an unmistakable form of learning, in the non-neural organism Physarum polycephalum. In our experiment, using chemotaxis as the behavioural output and quinine or caffeine as the stimulus, we showed that P. polycephalum learnt to ignore quinine or caffeine when the stimuli were repeated, but responded again when the stimulus was withheld for a certain time. Our results meet the principle criteria that have been used to demonstrate habituation: responsiveness decline and spontaneous recovery. To distinguish habituation from sensory adaptation or motor fatigue, we also show stimulus specificity. Our results point to the diversity of organisms lacking neurons, which likely display a hitherto unrecognized capacity for learning, and suggest that slime moulds may be an ideal model system in which to investigate fundamental mechanisms underlying learning processes. Besides, documenting learning in non-neural organisms such as slime moulds is centrally important to a comprehensive, phylogenetic understanding of when and where in the tree of life the earliest manifestations of learning evolved.

学习被定义为经验引发的行为改变，迄今为止几乎仅在具备神经元的多细胞生物中得到研究。目前关于无神经元多细胞生物的学习证据极为匮乏，仅少数明确的学习相关报道见于单细胞生物中。本研究在无神经元生物多头绒泡菌（Physarum polycephalum）中证实了习惯化（habituation）——一种明确无误的学习形式。本实验以趋化性作为行为输出指标，以奎宁或咖啡因作为刺激物，结果显示多头绒泡菌经重复刺激后会逐渐忽视奎宁或咖啡因，但当刺激暂停一段时间后，其响应能力会再次恢复。本研究结果符合验证习惯化的核心判定标准：响应性下降与自发恢复。为区分习惯化与感觉适应或运动疲劳，我们同时证实了刺激特异性。本研究结果表明，缺乏神经元的生物类群可能具备此前未被认知的学习能力，而黏菌或许是探究学习过程底层核心机制的理想模型系统。此外，记录黏菌这类无神经元生物的学习行为，对于全面、系统地从系统发育角度理解学习在生命之树上最早出现的时间与演化位置，具有核心意义。