The role of cerebellar plasticity has been increasingly recognized in learning. The privileged relationship between the cerebellum and the inferior olive offers an ideal circuit for attempting to integrate the numerous evidences of neuronal plasticity into a translational perspective. The high learning capacity of the Purkinje cells specifically controlled by the climbing fiber represents a major element within the feed-forward and feedback loops of the cerebellar cortex. Reciprocally connected with the basal ganglia and multimodal cerebral domains, this cerebellar network may realize fundamental functions in a wide range of behaviors. This review will outline the current understanding of three main experimental paradigms largely used for revealing cerebellar functions in behavioral learning: (1) the vestibuloocular reflex and smooth pursuit control, (2) the eyeblink conditioning, and (3) the sensory envelope plasticity. For each of these experimental conditions, we have critically revisited the chain of causalities linking together neural circuits, neural signals, and plasticity mechanisms, giving preference to behaving or alert animal physiology. Namely, recent experimental approaches mixing neural units and local field potentials recordings have demonstrated a spike timing dependent plasticity by which the cerebellum remains at a strategic crossroad for deciphering fundamental and translational mechanisms from cellular to network levels. 1. Introduction Recent evidences show that the cerebellum plays a key role in motor and nonmotor domains through a great number of cerebro-cerebellar closed loops [1] (Figure 1) that sustain different forms of learning [2–9]. In this context, it is widely admitted that synaptic plasticity underlies learning and memory [10–15] and that the Purkinje cell (PC), which is the sole output neuron of the cerebellar cortex, can learn up to 5 kilobytes of information corresponding to 40,000 input-output associations [16]. This high learning capacity of the PC promotes this type of neuron at the first place for revisiting the different approaches already performed in studying plasticity in cerebellum. Figure 1: Schematic diagram of the circuits interconnecting the olivocerebellum, the thalamus, the basal ganglia, the pontine nuclei, the cerebral cortex, and the spinal cord. The part of the circuit showing anatomical links between the basal-ganglia and the cerebellum is adapted from recent anatomical experiments using retrograde transneuronal transport of rabies virus from injections into the cerebellar cortex and in nuclei of
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