Associative learning in the protozoan Stentor coeruleus

The capacity for associative learning in protozoa has been a matter of longstanding controversy. In a series of Pavlovian conditioning experiments with the ciliate Stentor coeruleus, we show that temporally pairing weak and strong mechanical stimuli results in a transiently enhanced contraction response to the weak stimulus. Control experiments rule out several alternative explanations, such as non-associative sensitization or arousal. Parametric manipulation of the conditioning protocol's temporal structure revealed a systematic dependence of learning on the inter-trial and inter-stimulus intervals, though not in the form classically observed in animals. A simple mathematical model, combining associative learning with habituation, can explain why enhancement is transient, and accurately fits the learning curve at the aggregate level. We conclude that Stentor coeruleus appears capable of associative learning, suggesting an ancient evolutionary origin that preceded the emergence of multicellular nervous systems.