Cerebellar damage impairs long-term but not short-term sensorimotor memory

Abstract

The cerebellum is critical for sensorimotor learning. The specific contribution that it makes, however, remains unclear. Inspired by the classic finding that, for declarative memories, medial temporal lobe structures provide a gateway to the formation of long-term memory but are not required for short-term memory, we hypothesized that, for sensorimotor memories, the cerebellum may play an analogous role. Here we studied the sensorimotor learning of individuals with severe ataxia from cerebellar degeneration. We dissected the memories they formed during sensorimotor learning into a short-term temporally-volatile component, that decays rapidly with a time constant of just 15-20sec and thus cannot lead to long-term retention, and a longer-term temporally-persistent component that is stable for 60 sec or more and leads to long-term retention. Remarkably, we find that these individuals display dramatically reduced levels of temporally-persistent sensorimotor memory, despite spared and even elevated levels of temporally-volatile sensorimotor memory. In particular, we find both impairment that systematically increases with memory window duration over shorter memory windows (<12 sec) and near-complete impairment of memory maintenance over longer memory windows (>25 sec). This dissociation uncovers a new role for the cerebellum as a gateway for the formation of long-term but not short-term sensorimotor memories, mirroring the role of the medial temporal lobe for declarative memories. It thus reveals the existence of distinct neural substrates for short-term and long-term sensorimotor memory, and it explains both newly-identified trial-to-trial differences and long-standing study-to-study differences in the effects of cerebellar damage on sensorimotor learning ability. Significance StatementA key discovery about the neural underpinnings of memory, made more than half a century ago, is that long-term, but not short-term, memory formation depends on neural structures in the brains medial temporal lobe (MTL). However, this dichotomy holds only for declarative memories - memories for explicit facts such as names and dates - as long-term procedural memories - memories for implicit knowledge such as sensorimotor skills - are largely unaffected even with substantial MTL damage. Here we demonstrate that the formation of long-term, but not short-term, sensorimotor memory depends on a neural structure known as the cerebellum, and we show that this finding explains the variability previously reported in the extent to which cerebellar damage affects sensorimotor learning.