Significance The information that one region of the brain transmits to another is usually viewed through the lens of firing rates. However, if the output neurons could vary the timing of their spikes, then, through synchronization, they would spotlight information that may be critical for control of behavior. Here we report that, in the cerebellum, Purkinje cell populations that share a preference for error convey, to the nucleus, when to decelerate the movement, by reducing their firing rates and temporally synchronizing the remaining spikes.

The common marmoset ( Callithrix jacchus) is a promising new model for study of neurophysiological basis of behavior in primates. Like other primates, it relies on saccadic eye movements to monitor and explore its environment. Previous reports have demonstrated some success in training marmosets to produce goal-directed actions in the laboratory. However, the number of trials per session has been relatively small, thus limiting the utility of marmosets as a model for behavioral and neurophysiological studies. In this article, we report the results of a series of new behavioral training and neurophysiological protocols aimed at increasing the number of trials per session while recording from the cerebellum. To improve the training efficacy, we designed a precisely calibrated food regulation regime that motivates the subjects to perform saccade tasks, resulting in ~1,000 reward-driven trials on a daily basis. We then developed a multichannel recording system that uses imaging to target a desired region of the cerebellum, allowing for simultaneous isolation of multiple Purkinje cells in the vermis. In this report, we describe 1) the design and surgical implantation of a computer tomography (CT)-guided, subject-specific head post, 2) the design of a CT- and MRI-guided alignment tool for trajectory guidance of electrodes mounted on an absolute encoder microdrive, 3) development of a protocol for behavioral training of subjects, and 4) simultaneous recordings from pairs of Purkinje cells during a saccade task. NEW & NOTEWORTHY Marmosets present the opportunity to investigate genetically based neurological disease in primates, in particular, diseases that affect social behaviors, vocal communication, and eye movements. All of these behaviors depend on the integrity of the cerebellum. We present training methods that better motivate the subjects, allowing for improved performance, and we also present electrophysiological techniques that precisely target the subject’s cerebellum, allowing for simultaneous isolation of multiple Purkinje cells.

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Analysis of electrophysiological data from Purkinje cells (P-cells) of the cerebellum presents unique challenges to spike sorting. Complex spikes have waveforms that vary significantly from one event to the next, raising the problem of misidentification. Even when complex spikes are detected correctly, the simple spikes may belong to a different P-cell, raising the danger of misattribution. To address these identification and attribution problems, we wrote an open-source, semi-automated software called P-sort, and then tested it by analyzing data from P-cells recorded in three species: marmosets, macaques, and mice. Like other sorting software, P-sort relies on nonlinear dimensionality reduction to cluster spikes. However, it also uses the statistical relationship between simple and complex spikes to merge disparate clusters and split a single cluster. In comparison with expert manual curation, occasionally P-sort identified significantly more complex spikes, as well as prevented misattribution of clusters. Three existing automatic sorters performed less well, particularly for identification of complex spikes. To improve development of analysis tools for the cerebellum, we provide labeled data for 313 recording sessions, as well as statistical characteristics of waveforms and firing patterns of P-cells in three species.

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