Neurons are generally considered to communicate information by increasing or decreasing their firing rate. However, in principle, they could in addition convey messages by using specific spatiotemporal patterns of spiking activities and silent intervals. Here, we review expanding lines of evidence that such spatiotemporal coding occurs in the cerebellum, and that the olivocerebellar system is optimally designed to generate and employ precise patterns of complex spikes and simple spikes during the acquisition and consolidation of motor skills. These spatiotemporal patterns may complement rate coding, thus enabling precise control of motor and cognitive processing at a high spatiotemporal resolution by fine-tuning sensorimotor integration and coordination.

The cerebellum refines the accuracy and timing of motor performance. How it encodes information to perform these functions is a major topic of interest. We performed whole cell and extracellular recordings of Purkinje cells (PCs) and cerebellar nuclei neurons (CNs) in vivo, while activating PCs with light in transgenic mice. We show for the first time that graded activation of PCs translates into proportional CN inhibition and induces rebound activity in CNs, which is followed by graded motor contractions timed to the cessation of the stimulus. Moreover, activation of PC ensembles led to disinhibition of climbing fiber activity, which coincided with rebound activity in CNs. Our data indicate that cessation of concerted activity in ensembles of PCs can regulate both timing and strength of movements via control of rebound activity in CNs.

The output of the cerebellar cortex is controlled by two main inputs, (i.e., the climbing fiber and mossy fiber-parallel fiber pathway) and activations of these inputs elicit characteristic effects in its Purkinje cells: that is, the so-called complex spikes and simple spikes. Target neurons of the Purkinje cells in the cerebellar nuclei show rebound firing, which has been implicated in the processing and storage of motor coordination signals. Yet, it is not known to what extent these rebound phenomena depend on different modes of Purkinje cell activation. Using extracellular as well as patch-clamp recordings, we show here in both anesthetized and awake rodents that simple and complex spike-like train stimuli to the cerebellar cortex, as well as direct activation of the inferior olive, all result in rebound increases of the firing frequencies of cerebellar nuclei neurons for up to 250 ms, whereas single-pulse stimuli to the cerebellar cortex predominantly elicit well-timed spiking activity without changing the firing frequency of cerebellar nuclei neurons. We conclude that the rebound phenomenon offers a rich and powerful mechanism for cerebellar nuclei neurons, which should allow them to differentially process the climbing fiber and mossy fiber inputs in a physiologically operating cerebellum.olivo-cerebellar loop | rebound firing | Purkinje cell | complex spikes | simple spikes N eurons in the cerebellar nuclei (CN) form the main output of the cerebellum (1). They include GABAergic neurons that provide an inhibitory feedback to the inferior olive (IO) and excitatory neurons that project to various other brainstem nuclei exerting motor control (2-4). In turn, each CN neuron receives a prominent inhibitory GABAergic input from tens of Purkinje cells, a substantial excitatory input from climbing fiber and mossy fiber collaterals, and a modest input from the local interneurons (4-7). Apart from the impact of these inputs, the firing pattern of CN neurons is largely determined by their intrinsic activities (4,(8)(9)(10)(11)(12)(13)(14). Interestingly, following inhibitory current injections or activation of their Purkinje cell input, CN neurons can show a "rebound" depolarization of the membrane potential, accompanied by action-potential firing (8, 11). Even though little is known about the prominence of rebound firing in the awake state, various models on cerebellar function consider this rebound phenomenon in the nuclei as an essential mechanism to process and store relevant information on motor coordination (15-18). The conductances that allow the rebound firing to emerge involve various types of Ca 2+ -channels, the distribution of which probably varies among the different types of neurons in the CN (8,11,14,(19)(20)(21)(22)(23). Regardless of the type of CN neuron, it is tempting to hypothesize that the climbing fibers and parallel fibers, which evoke complex spikes and simple spikes (24-27), respectively, have a differential impact on the generation of rebound activities in the CN neurons.To test this hypothe...