In vivo properties of cerebellar interneurons in the macaque caudal vestibular vermis

Abstract

We quantify both spontaneous and stimulus-driven responses of interneurons in lobules X (nodulus) and IXc,d (ventral uvula) of the caudal vermis during vestibular stimulation. Based on baseline firing, at least three types of neuronal populations could be distinguished. First, there was a group of very regular firing neurons with high mean discharge rates. Second, there was a group of low firing neurons with a range of discharge regularity. Third, we also encountered putative interneurons with discharge regularity and mean firing rates that were indistinguishable from those of physiologically identified Purkinje cells. The vestibular responses of putative interneurons were generally similar to those of Purkinje cells, thus encoding tilt, translation or mixtures of these signals. Mossy fibres showed unprocessed, otolith afferent-like properties. The cerebellar cortex is among the brain's most well-studied circuits and includes distinct classes of excitatory and inhibitory interneurons. Several studies have attempted to characterize the in vivo properties of cerebellar interneurons, yet little is currently known about their stimulus-driven properties. Here we quantify both spontaneous and stimulus-driven responses of interneurons in lobules X (nodulus) and IXc,d (ventral uvula) of the macaque caudal vermis during vestibular stimulation. Interneurons were identified as cells located >100 μm from the Purkinje cell layer that did not exhibit complex spikes. Based on baseline firing, three types of interneurons could be distinguished. First, there was a group of very regular firing interneurons with high mean discharge rates, which consistently encoded tilt, rather than translational head movements. Second, there was a group of low firing interneurons with a range of discharge regularity. This group had more diverse vestibular properties, where most were translation-selective and a few tilt- or gravitoinertial acceleration-selective. Third, we also encountered interneurons that were similar to Purkinje cells in terms of discharge regularity and mean firing rate. This group also encoded mixtures of tilt and translation signals. A few mossy fibres showed unprocessed, otolith afferent-like properties, encoding the gravitoinertial acceleration. We conclude that tilt- and translation-selective signals, which reflect neural computations transforming vestibular afferent information, are not only encountered in Purkinje cell responses. Instead, upstream interneurons within the cerebellar cortex are also characterized by similar properties, thus implying a widespread network computation.