Sensorimotor adaptation of vocal pitch is severely impaired in cerebellar ataxia

Abstract

Sensory errors, mismatches between predicted sensory outcomes of movement and reafferent sensory feedback, drive changes in the feedforward control of future motor behavior that correct for those errors. Across a wide variety of motor behaviors, individuals with cerebellar damage show impairments in these corrections, strongly suggesting a key role of the cerebellum in sensorimotor adaptation. However, the extent to which the cerebellum is involved in controlling vocal pitch is currently unknown. Crucially, vocal pitch differs in several ways from other systems that suggest it relies more on feedback than feedforward control. Adaptation itself also differs in vocal pitch: rather than the gradual build-up/decay of learning seen in other systems, pitch adaptation and de-adaptation are almost immediate. Together, this questions whether adaptation in vocal pitch relies on the same mechanism as other motor domains. Here, we test the hypothesis that the cerebellum underlies sensorimotor adaptation in vocal pitch, testing the domain-generality of this neurocomputational process. In both sustained vocalization and a more natural word production task, individuals with cerebellar ataxia fail to adapt to external auditory perturbation of vocal pitch. The complete lack of adaptation observed, compared to the impaired but present adaptation seen in other systems, suggest that the cerebellum plays an especially critical role in maintaining accurate control of vocal pitch. Conversely, we failed to detect a previously observed increase in online compensation to vocal pitch errors in ataxia, potentially suggesting this may be an idiosyncratic change in control rather than a common trait in this population. Significance statementWhen exposed to external perturbations of vocal pitch, individuals with cerebellar ataxia fail to adapt their produced pitch to oppose the perturbation. These results highlight the critical role of the cerebellum in driving adaptation across motor domains, even for motor behaviors that are thought to rely more on feedback compared to feedforward control, such as pitch. Conversely, and despite a large cohort, we failed to replicate previous findings of enhanced online corrections for pitch perturbations in ataxia, suggesting that any such increases are likely due to individual-specific changes in motor function in response to cerebellar-induced control deficits rather than being directly related to cerebellar damage itself.