The cerebellum as a predictor of neural messages—I. The stable estimator hypothesis

Abstract

To describe how the central nervous system combines sensory messages, the hypothesis of a “stable estimator” is proposed: the central nervous system would construct internal estimates of the physical variables characterizing the body movements (e.g. head rotational velocity in space), while a regulating circuit would optimize the process of estimation of each variable, according to the available information and the overall performances of the sensorimotor reactions. The stable estimator of each variable would be embedded in a definite folium of the cerebellar cortex and the related cerebellar and brainstem nuclei. It would be controlled by the related part of the inferior olive. The estimate of each physical variable would be constructed by complementing the message from a dedicated sensory system (e.g. the semi-circular canals, which measure head rotational velocity in space) by neural messages related to the same variable (e.g. eye velocity in the head and retinal slip). Thus, the estimate would be accurate over the widest possible physiological ranges of frequency and velocity. The complementing signals would result from combining estimates of other variables (such as gaze velocity and eye velocity in the orbit), according to rules reproducing the relationships between physical variables. From the same complementing signals, the message from the dedicated sensory system would be predicted, and it is argued that this predictive function resides in the cerebellar cortex. The inferior olive would compare an actual signal about the performance of a sensorimotor reaction to signals of expected performance, computed from the various internal estimates of the variables which determine this performance. Any erroneous setting in a stable estimator would cause differences between the actual and the expected values. Then the inferior olive would compute an error signal directing compensatory functional plasticity. Finally, the whole estimating circuit would be regulated so that the internal coherence between neural messages and the performance of sensorimotor reactions would be achieved. Anatomical identifications and rules of functional plasticity are proposed.