Cerebellar complex spikes multiplex complementary behavioral information

Purkinje cell (PC) discharge, the only output of cerebellar cortex, involves two types of action potentials, high-frequency simple spikes (SSs) and low-frequency complex spikes (CSs). While there is consensus that SSs convey information needed to optimize movement kinematics, the function of CSs, determined by the PC´s climbing fibre input, remains controversial. While initially thought to be specialized in reporting information on motor error for the subsequent amendment of behavior, CSs seem to contribute to other aspects of motor behavior as well. When faced with the bewildering diversity of findings and views unraveled by highly specific tasks one may wonder if there is just one true function with all the other attributions wrong? Or is the diversity of findings a reflection of distinct pools of PCs, each processing specific streams of information conveyed by climbing fibres? With these questions in mind, we recorded CSs from the monkey oculomotor vermis deploying a repetitive saccade task that entailed sizable motor errors as well as small amplitude saccades, correcting them. We demonstrate that in addition to carrying error-related information, CSs carry information on the metrics of both primary and small corrective saccades in a time-specific manner, with changes in CS firing probability coupled with changes in CS duration. Furthermore, we also found CS activity that seemed to predict the upcoming events. Hence PCs receive a multiplexed climbing fibre input that merges complementary streams of information on the behavior, separable by the recipient PC because they are staggered in time.

浦肯野细胞（Purkinje cell）作为小脑皮层的唯一输出神经元，其放电活动包含两类动作电位：高频简单锋电位（simple spikes，SSs）与低频复杂锋电位（complex spikes，CSs）。学界普遍认为简单锋电位承载了优化运动学参数所需的信息，但由浦肯野细胞攀缘纤维（climbing fibre）输入所决定的复杂锋电位的功能仍存在争议。尽管最初认为复杂锋电位专门用于报告运动误差信息以指导后续行为修正，现有研究表明其同样参与运动行为的其他方面。当面对高度特异性实验任务所揭示的纷繁芜杂的研究发现与学术观点时，人们不禁会思考：是否仅存在一种正确的功能，而其他所有归因均为谬误？抑或是研究结果的多样性反映了不同亚群的浦肯野细胞——每个亚群均处理由攀缘纤维传递的特定信息流？带着这些疑问，我们采用一项涉及显著运动误差以及用于修正误差的小幅振幅扫视的重复性扫视任务，记录了猴动眼小脑蚓部的复杂锋电位活动。我们证实，复杂锋电位除携带误差相关信息外，还以时间特异性方式编码初级扫视与修正性小幅扫视的运动学特征，其放电概率的变化与持续时长的改变紧密耦合。此外，我们还观测到可预测即将发生事件的复杂锋电位活动。综上，浦肯野细胞接收的是多路复用的攀缘纤维输入，该输入整合了关于行为的互补信息流；由于这些信息流在时间维度上存在错位，因此可被接收的浦肯野细胞加以区分。