Cerebellar, parietal, and frontal cortex exert distinct causal influences on cortical population codes supporting working memory

Abstract

Working memory, the transient maintenance and manipulation of information, is fundamental to human cognition. While working memory is typically thought to rely on frontoparietal cortex, the cerebellum communicates with association cortex through closed-loop cerebro-cerebellar pathways and is well positioned to influence cortical dynamics supporting cognition. It is currently unknown whether cerebellar processing is causally necessary for the maintenance of visual information and whether cortical population coding is dependent on cerebellum. We combined functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation (TMS) of frontal, parietal, and cerebellar cortex in humans. Using a generative model of population receptive fields, we show that cerebellar perturbation impairs spatial working memory recall and broadly degrades cortical spatial tuning. Direct comparisons revealed dissociable effects on population coding: cerebellar perturbation preferentially reduced stimulus-specific gain in early visual cortex, parietal perturbation preferentially suppressed stimulus-independent visual responses, and frontal perturbation preferentially increased response variability across higher-order visual, parietal, and frontal regions. These findings demonstrate that intact cerebellar function is necessary for maintaining cortical working memory representations and that cerebellar, parietal, and frontal nodes support working memory fidelity via distinct mechanisms.