Tactile stimulation transiently disrupts encoding of whisker position by cerebellar molecular layer interneuron ensembles

Abstract

Molecular layer interneurons (MLIs) within the cerebellar cortex mediate feed-forward inhibition onto Purkinje cells, positioning them as pivotal modulators of cerebellar output. We asked how motor patterns and salient sensory input influence MLI population activity during active whisking and tactile interactions. Utilizing two-photon calcium imaging combined with high-speed videography, we examined MLI population dynamics in awake, behaving mice engaged in voluntary whisker movements. Our results demonstrate that during free whisking, MLI population activity reliably tracks whisker position, yielding uniform graded responses that provide stable and precise representations over time. Tactile contact with external stimuli evokes additional activation in a subset of MLIs. Sensory input transiently disrupts the linear relationship between MLI activity and whisker position and may account for rapid synchronous inhibition of Purkinje cell spiking activity following tactile stimulation. These findings indicate that MLIs in Crus 1 maintain an accurate internal model of whisker position which is perturbed upon encountering obstacles. This disruption likely reflects the integration of sensory feedback, disrupting predictive signals that are subsequently passed forward to Purkinje cells. Such signals can alert the brain to novel happenings and be used to update motor commands, thereby contributing to cerebellar function in response to environmental changes.