What Features of Limb Movements are Encoded in the Discharge of Cerebellar Neurons?

Abstract

This review examines the signals encoded in the discharge of cerebellar neurons during voluntary arm and hand movements, assessing the state of our knowledge and the implications for hypotheses of cerebellar function. The evidence for the representation of forces, joint torques, or muscle activity in the discharge of cerebellar neurons is limited, questioning the validity of theories that the cerebellum directly encodes the motor command. In contrast, kinematic parameters such as position, direction, and velocity are widely and robustly encoded in the activity of cerebellar neurons. These findings favor hypotheses that the cerebellum plans or controls movements in a kinematic framework, such as the proposal that the cerebellum provides a forward internal model. Error signals are needed for on-line correction and motor learning, and several hypotheses postulate the need for their representations in the cerebellum. Error signals have been described mostly in the complex spike discharge of Purkinje cells, but no consensus has emerged on the exact information signaled by complex spikes during limb movements. Newer studies suggest that simple spike firing may also encode error signals. Finally, Purkinje cells located more posterior and laterally in the cerebellar cortex and dentate neurons encode nonmotor, task-related signals such as visual cues. These results suggest that cerebellar neurons provide a complement of information about motor behaviors. We assert that additional single unit studies are needed using rich movement paradigms, given the power of this approach to directly test specific hypotheses about cerebellar function.

Genetic silencing of olivocerebellar synapses causes dystonia-like behaviour in mice

“…Climbing fibre activity is thought to be a central requirement for cerebellar functions, ranging from ongoing motor behaviour38 to learning3940 to error correction41. By extrapolation, climbing fibre function could be predicted to have a major impact on motor disease.…”

The Roles of the Olivocerebellar Pathway in Motor Learning and Motor Control. A Consensus Paper

“…Support for this hypothesis is the CS modulation observed during eye movements in relation to retinal slip, smooth pursuit adaptation and induced saccade errors [39–43]. During reaching CSs are evoked by end point errors, redirection, unexpected loads, and adaptation to visuomotor transformations (for review, see [44]). However, numerous other studies found no clear relationship between motor errors and CS activity or the discharge of neurons in the inferior olive, the origin of the climbing fiber projection, either during eye or limb movements (see [45]).…”

Physiologic Changes Associated with Cerebellar Dystonia

“…Only a subset of cerebellar output neurons are presumed to directly regulate motor activity of the limb, with others that discharge in relation to joint position, and the direction of the intended next movement [38]. Although some investigators favor the view that the cerebellum solely plans and controls movements in a kinematic framework, without directly encoding force-related parameters [39], at least a subset of cerebellar output neurons do appear to directly activate muscle groups as evidenced by electrical stimulation of interposed and dentate nuclei in primates [40]. Also, optogenetic manipulation of Purkinje neurons in mice shows that inhibiting Purkinje cell firing can cause muscle contraction[41, 42].…”