Purkinje Cell Activity in the Medial and Lateral Cerebellum During Suppression of Voluntary Eye Movements in Rhesus Macaques

Abstract

Volitional suppression of responses to distracting external stimuli enables us to achieve our goals. This volitional inhibition of a specific behavior is supposed to be mainly mediated by the cerebral cortex. However, recent evidence supports the involvement of the cerebellum in this process. It is currently not known whether different parts of the cerebellar cortex play differential or synergistic roles in the planning and execution of this behavior. Here, we measured Purkinje cell (PC) responses in the medial and lateral cerebellum in two rhesus macaques during pro- and anti-saccade tasks. During an antisaccade trial, non-human primates (NHPs) were instructed to make a saccadic eye movement away from a target, rather than toward it, as in prosaccade trials. Our data show that the cerebellum plays an important role not only during the execution of the saccades but also during the volitional inhibition of eye movements toward the target. Simple spike (SS) modulation during the instruction and execution periods of pro- and anti-saccades was prominent in PCs of both the medial and lateral cerebellum. However, only the SS activity in the lateral cerebellar cortex contained information about stimulus identity and showed a strong reciprocal interaction with complex spikes (CSs). Moreover, the SS activity of different PC groups modulated bidirectionally in both of regions, but the PCs that showed facilitating and suppressive activity were predominantly associated with instruction and execution, respectively. These findings show that different cerebellar regions and PC groups contribute to goal-directed behavior and volitional inhibition, but with different propensities, highlighting the rich repertoire of the cerebellar control in executive functions.

Encoding of cerebellar dentate neuron activity during visual attention in rhesus macaques

“…Many DN neurons respond in a visual direction-or movement direction-selective manner more than half a second before an upcoming saccade, with relatively short latencies after the animal receives the visual information that instructs saccade direction. The activity of DN cells often bridged different experimental epochs and frequently showed both upbound and downbound modulations (De Zeeuw, 2021), similar to PCs in the lateral cerebellum that project to the DN (Avila et al, 2022). In these ways, multi-modality appears to be a common property of neurons in the lateral cerebellum.…”

“…After a delay, the primates had to move their eyes to a virtual point in space dependent on the cue implied by the peripheral C-stimulus. The spatial and temporal dissociation of cue and action in this task allows us to dissociate neural activity related to the visual and attentional processes from that related to motor coordination (Avila et al, 2022;Goldberg and Segraves, 1987). Our data reveal that individual DN cells can encode both the direction of the visual cue and the associated direction of the subsequent saccade, suggesting that different task-specific activations in the cerebellar cortex may be relayed downstream to the same target neurons in the cerebellar nuclei.…”

“…Two adult male non-human primates (NHPs, Macaca mulatta), referred to as Mi and Mo, were used in this study. Before being subjected to the peripheral Landolt C saccade task of the current study, both of them were used for two other studies, one on glissade control and another one on mechanisms underlying anti-saccades (Avila et al, 2022;.…”

“…Four months later, under the same anesthesia conditions, a custom-made 40 mm-wide chamber was implanted to gain access to the cerebellum. Animals recovered for at least 21 days before behavioral training and testing (for more details on surgical procedures, see (Avila et al, 2022;Flierman et al, 2019).…”

Fundamental processes in sensorimotor learning: Reasoning, refinement, and retrieval

“…How can we examine the neural correlates of motor skill acquisition? Although numerous approaches exist ( Avila et al, 2022 ; Calame et al, 2023 ; Darmohray et al, 2019 ; Georgopoulos et al, 1989 ; Vyas et al, 2020 ), systems neuroscientists usually do not fully know the causal relationship between neural activity and behavior. Conversely, in a brain–computer interface (BCI) paradigm, the precise causal relationship between neural activity and behavior is determined by the BCI mapping, set by the experimenter.…”