Representation of limb kinematics in Purkinje cell simple spike discharge is conserved across multiple tasks

Abstract

Encoding of movement kinematics in Purkinje cell simple spike discharge has important implications for hypotheses of cerebellar cortical function. Several outstanding questions remain regarding representation of these kinematic signals. It is uncertain whether kinematic encoding occurs in unpredictable, feedback-dependent tasks or kinematic signals are conserved across tasks. Additionally, there is a need to understand the signals encoded in the instantaneous discharge of single cells without averaging across trials or time. To address these questions, this study recorded Purkinje cell firing in monkeys trained to perform a manual random tracking task in addition to circular tracking and center-out reach. Random tracking provides for extensive coverage of kinematic workspaces. Direction and speed errors are significantly greater during random than circular tracking. Cross-correlation analyses comparing hand and target velocity profiles show that hand velocity lags target velocity during random tracking. Correlations between simple spike firing from 120 Purkinje cells and hand position, velocity, and speed were evaluated with linear regression models including a time constant, τ, as a measure of the firing lead/lag relative to the kinematic parameters. Across the population, velocity accounts for the majority of simple spike firing variability (63 ± 30% of R(adj)(2)), followed by position (28 ± 24% of R(adj)(2)) and speed (11 ± 19% of R(adj)(2)). Simple spike firing often leads hand kinematics. Comparison of regression models based on averaged vs. nonaveraged firing and kinematics reveals lower R(adj)(2) values for nonaveraged data; however, regression coefficients and τ values are highly similar. Finally, for most cells, model coefficients generated from random tracking accurately estimate simple spike firing in either circular tracking or center-out reach. These findings imply that the cerebellum controls movement kinematics, consistent with a forward internal model that predicts upcoming limb kinematics.

Functional and Structural Correlates of Motor Speed in the Cerebellar Anterior Lobe

“…Functional activity in the cerebellum during repeated foot movements agrees with the cerebellar homunculus within the anterior lobe [54]. Along with the study of Hewitt and colleagues (2011) our results suggest that the ability to move as fast as possible is bound to the capability of generating highest possible discharge rates in a certain population of Purkinje cells [12]. Due to the concept of spatial summation at the dendritic tree, which in part underlies volumetric differences [55], it is likely that this ability is manifested in a neuroanatomical correlate of increased grey matter volume in the cerebellar anterior lobe.…”

“…Indeed, the cerebellum is characterised as the neural site which encodes speed information and provides a forward internal model to plan or control movements in a kinematic framework [10]. According to this, several animal studies observed correlations between discharge rate of Purkinje cells and movement velocity [11], [12]. In humans, it could be shown that patients with cerebellar lesions are not able to generate fast arm speeds compared to healthy controls [13].…”

The cerebellum for jocks and nerds alike

“…Therefore, we evaluated Purkinje cell firing during random tracking and verified that position, velocity and speed of the limb (denoted in Figure 1B by the C subscripted variables) were statistically independent (Hewitt et al, 2011). For a large majority of Purkinje cells, simple spike firing is modulated in relation to these kinematic parameters.…”

Differential effects of ketamine/xylazine anesthesia on the cerebral and cerebellar cortical activities in the rat

“…The first is rate coding in which the simple spike frequency is varied. It has been shown that the Purkinje simple spike frequency is correlated with arm kinematic and dynamic variables (Albus 1971;Dean et al 2010;Ebner et al 2011;Hewitt et al 2011;Lisberger 2009;McElvain et al 2010;Pasalar et al 2006). The second is spatiotemporal coding where the spike synchrony between multiple Purkinje cells is the mechanism for propagation of information.…”