Cerebellar Motor Learning: When Is Cortical Plasticity Not Enough?

Abstract

Classical Marr-Albus theories of cerebellar learning employ only cortical sites of plasticity. However, tests of these theories using adaptive calibration of the vestibulo–ocular reflex (VOR) have indicated plasticity in both cerebellar cortex and the brainstem. To resolve this long-standing conflict, we attempted to identify the computational role of the brainstem site, by using an adaptive filter version of the cerebellar microcircuit to model VOR calibration for changes in the oculomotor plant. With only cortical plasticity, introducing a realistic delay in the retinal-slip error signal of 100 ms prevented learning at frequencies higher than 2.5 Hz, although the VOR itself is accurate up to at least 25 Hz. However, the introduction of an additional brainstem site of plasticity, driven by the correlation between cerebellar and vestibular inputs, overcame the 2.5 Hz limitation and allowed learning of accurate high-frequency gains. This “cortex-first” learning mechanism is consistent with a wide variety of evidence concerning the role of the flocculus in VOR calibration, and complements rather than replaces the previously proposed “brainstem-first” mechanism that operates when ocular tracking mechanisms are effective. These results (i) describe a process whereby information originally learnt in one area of the brain (cerebellar cortex) can be transferred and expressed in another (brainstem), and (ii) indicate for the first time why a brainstem site of plasticity is actually required by Marr-Albus type models when high-frequency gains must be learned in the presence of error delay.

Author Summary

Our ability to learn skilled movements depends crucially on the cerebellum, hence understanding cerebellar plasticity is central to theories of motor learning. The adaptation of the vestibulo-ocular reflex (VOR) is often used to test these theories. This reflex stabilizes the retinal image by moving the eyes to compensate for head movements signaled by the vestibular system. There is a long-standing puzzle in that classical Marr-Albus theories of VOR adaptation only require sites of plasticity in cerebellar cortex whereas experiment reveals plasticity in both cerebellar cortex and brainstem. We resolve this puzzle by showing that unavoidable delays in processing retinal slip severely limit cerebellar performance at high frequencies but that introducing a second brainstem site of plasticity driven by the correlation between cerebellar and vestibular inputs overcomes this limitation. Hence a second site of plasticity is required by Marr-Albus models for high-frequency learning in the presence of delay. The plasticity mechanism we describe is of general interest because it provides a biologically plausible route by which motor information learnt in one brain area (cerebellar cortex) can be transferred to and expressed in another area (the brain stem).