Learning from the past: a reverberation of past errors in the cerebellar climbing fiber signal

The cerebellum allows us to rapidly adjust motor behavior to the needs of the situation. It is commonly assumed that cerebellum-based motor learning is guided by the difference between the desired and the actual behavior, i.e., by error information. Not only immediate but also future behavior will benefit from an error because it induces lasting changes of parallel fiber synapses on Purkinje cells (PCs), whose output mediates the behavioral adjustments. Olivary climbing fibers, likewise connecting with PCs, are thought to transport information on instant errors needed for the synaptic modification yet not to contribute to error memory. Here, we report work on monkeys tested in a saccadic learning paradigm that challenges this concept. We demonstrate not only a clear complex spikes (CS) signature of the error at the time of its occurrence but also a reverberation of this signature much later, before a new manifestation of the behavior, suitable to improve it.

小脑（cerebellum）可使我们依据情境需求快速调整运动行为。学界普遍认为，基于小脑的运动学习由预期行为与实际行为之间的差值——即错误信息——所引导。错误不仅能使当下行为获益，还可惠及未来行为：因为错误会诱发浦肯野细胞（Purkinje cells，PCs）上平行纤维突触的持久性改变，而浦肯野细胞的输出正是介导行为调整的核心通路。同样与浦肯野细胞形成连接的下橄榄核攀缘纤维（Olivary climbing fibers），被认为仅负责传递突触修饰所需的即时错误信息，却不参与错误记忆的形成。本研究通过眼跳运动学习范式（saccadic learning paradigm）对猕猴开展实验，所得结果对这一传统认知提出了挑战。我们不仅观测到错误发生时清晰的复杂锋电位（complex spikes，CS）特征信号，还发现该特征信号会在行为新一次表现前的较长时段内出现迟发性回响，从而助力行为优化。