The cerebellum specializes for language even in the absence of contralateral neocortical inputs

Abstract

Long considered a structure dedicated primarily to motor control, the cerebellum is now known to contain regions that respond selectively to language. However, how cerebellar language specialization emerges during development remains unknown. The prevailing proposal is that cerebellar functional specialization critically depends on inputs from the contralateral neocortex, received through well-established reciprocal cortico-cerebellar connections. Here, we test this proposal in two individuals with atypical brain development: EG, a right-handed woman who lacks most of her left temporal lobe (presumably from birth) and whose neocortical language network resides in her right hemisphere, and C1, an individual missing the entire left cerebral hemisphere from birth. Using precision functional MRI in EG and a cohort of 74 typically-developing adults, we find that EG's cerebellar language network shows a strong left-hemispheric bias, mirroring the atypical lateralization of language in her cerebral cortex, while preserving canonical topography and response profiles of the language-dominant cerebellar regions. Critically, however, EG's right cerebellar hemisphere also responds to language and even contains a language-selective region despite the absence of language regions in the neocortical left hemisphere. We replicate these cerebellar findings in C1, a more extreme case who is missing the entire left hemisphere. These results show that the cerebellum develops language sensitivity despite the absence of contralateral inputs in the face of early injury. Together, these findings challenge the view that cerebellar specialization critically requires contralateral neocortical inputs, and point instead to some degree of intrinsic neocortex-independent cerebellar organization.