High Cognitive Violation of Expectations is Compromised in Cerebellar Ataxia

While traditionally considered a motor structure, the cerebellum is also involved in cognition. However, the underlying cognitive mechanisms through which the cerebellum contributes to evolutionarily novel cognitive abilities remain poorly understood. Another open question is how this structure contributes to a core unifying mechanism across domains. Motivated by the evolutionary principle of neural reuse, we suggest that a successful account of cerebellar contributions to higher cognitive domains will build on the structures established role in motor behaviors. We conducted a series of neuropsychological experiments, assessing selective impairments in participants with cerebellar ataxia (CA) compared to neurotypicals in solving sequential discrete problems. In three experiments, participants were asked to solve symbolic subtraction, alphabet letter transformation, and novel artificial grammar problems, which were expected or unexpected. The CA group exhibited a disproportionate cost when comparing expected problems to unexpected problems, suggesting that the cerebellum is critical for violation of expectations (VE) across tasks. The CA group impairment was not found either when the complexity of the problem increased or in conditions of uncertainty. Together, these results demonstrate a possible causal role for the human cerebellum in higher cognitive abilities. VE might be a unifying cerebellar-dependent mechanism across motor and cognitive domains. Significance StatementWhile the cerebellum, a phylogenetically ancient brain region, is traditionally viewed as a motor structure, evidence suggests its involvement in cognition. However, the mechanisms by which the cerebellum supports evolutionarily novel cognitive abilities remain poorly understood. In addition, despite theoretical proposals, direct evidence for the cerebellums contribution to a core unifying mechanism across non-motor domains is lacking. Drawing on the principle of neural reuse, we present neuropsychological evidence highlighting the cerebellums causal role in symbolic arithmetic reasoning, alphabet transformation, and grammar problems via violation of expectations processes. The results offer a new perspective on how, rather than merely if, the cerebellum contributes to higher cognition, suggesting a constraint on its role in cognitive domains.