The brain continuously estimates the state of body and environment, with specific regions that are thought to act as Bayesian estimator, optimally integrating noisy and delayed sensory feedback with sensory predictions generated by the cerebellum. In control theory, Bayesian estimators are usually implemented using high-level representations. In this work, we designed a new spike-based computational model of a Bayesian estimator. The state estimator receives spiking activity from two neural populations encoding the sensory feedback and the cerebellar prediction, and it continuously computes the spike variability within each population as a reliability index of the signal these populations encode. The state estimator output encodes the current state estimate. We simulated a reaching task at different stages of cerebellar learning. The activity of the sensory feedback neurons encoded a noisy version of the trajectory after actual movement, with an almost constant intrapopulation spiking variability. Conversely, the activity of the cerebellar output neurons depended on the phase of the learning process. Before learning, they fired at their baseline not encoding any relevant information, and the variability was set to be higher than that of the sensory feedback (more reliable, albeit delayed). When learning was complete, their activity encoded the trajectory before the actual execution, providing an accurate sensory prediction; in this case, the variability was set to be lower than that of the sensory feedback. The state estimator model optimally integrated the neural activities of the afferent populations, so that the output state estimate was primarily driven by sensory feedback in prelearning and by the cerebellar prediction in postlearning. It was able to deal even with more complex scenarios, for example, by shifting the dominant source during the movement execution if information availability suddenly changed. The proposed tool will be a critical block within integrated spiking, brain-inspired control systems for simulations of sensorimotor tasks.

A nerve cell receives multiple inputs from upstream neurons by way of its synapses. Neuron processing functions are thus influenced by changes in the biophysical properties of the synapse, such as long-term potentiation (LTP) or depression (LTD). This observation has opened new perspectives on the biophysical basis of learning and memory, but its quantitative impact on the information transmission of a neuron remains partially elucidated. One major obstacle is the high dimensionality of the neuronal input-output space, which makes it unfeasible to perform a thorough computational analysis of a neuron with multiple synaptic inputs. In this work, information theory was employed to characterize the information transmission of a cerebellar granule cell over a region of its excitatory input space following synaptic changes. Granule cells have a small dendritic tree (on average, they receive only four mossy fiber afferents), which greatly bounds the input combinatorial space, reducing the complexity of information-theoretic calculations. Numerical simulations and LTP experiments quantified how changes in neurotransmitter release probability ( p ) modulated information transmission of a cerebellar granule cell. Numerical simulations showed that p shaped the neurotransmission landscape in unexpected ways. As p increased, the optimality of the information transmission of most stimuli did not increase strictly monotonically; instead it reached a plateau at intermediate p levels. Furthermore, our results showed that the spatiotemporal characteristics of the inputs determine the effect of p on neurotransmission, thus permitting the selection of distinctive preferred stimuli for different p values. These selective mechanisms may have important consequences on the encoding of cerebellar mossy fiber inputs and the plasticity and computation at the next circuit stage, including the parallel fiber–Purkinje cell synapses.