Control of tongue movements by the cerebellum

Johns Hopkins University, Baltimore MD

Investigators

Abstract

We use our tongue to shape the air and generate sounds in order to communicate, and we use our tongue to evaluate food morsels and transport them through the oral cavity in order to eat. These are skillful acts that involve activation of over 100 muscles 1, producing movements that are fundamental to our existence. Damage to the cerebellum profoundly disrupts the ability to control our tongue, resulting in abnormal muscle activation patterns 2 that resemblance ataxia of the arm 3. But unlike the arm, control of tongue movements by the cerebellum has been difficult to study because of the limited access that we have for kinematic measurements. As a result, from a behavioral perspective, we have no standard task to measure learning of tongue movements, and from a neurophysiological perspective, despite the fact that dysarthria is a core feature of cerebellar disease 4, there are very few studies that have quantified lingual control by the cerebellum in non-human primates 5,6. Here, we propose to develop the marmoset model for the study of the cerebellum in lingual control. We think that these animals can significantly contribute to the study of tongue control because they have an exceptionally long tongue 7, and can skillfully use it to make target-directed movements, during which we can measure kinematics using standard marker-less tracking tools 8,9. Moreover, because marmosets are skilled in bending their tongue so to burrow into small holes, we can develop behavioral paradigms that involve precise endpoint control as well as error-dependent learning. Thus, we propose to develop novel behavioral paradigms in marmosets and combine them with neurophysiological studies of their cerebellum. We have two scientific questions: 1) Do phylogenetically newer parts of the cerebellum differ in their contributions to control of the tongue than the older regions? To answer this question, we will employ suppression of Purkinje cells during target-directed tongue movements and measure how this alters the tongue’s trajectory. We will compare these effects in the vermis, vs. the paravermis regions. We predict that whereas in the vermis, P-cell suppression affects simple protraction-retraction dimension of the tongue’s trajectory, disrupting the ability to stop at the target, in the paravermal regions a similar suppression will produce medial-lateral deviations, disrupting the ability to bend the tongue at oblique angles. Next, we ask: 2) How does the cerebellum contribute to learning of tongue movements? To answer this question, we will develop methods to induce errors for target-directed tongue movements, then record how Purkinje cells encode those errors and learn from them. We will build a robotic system that displaces the target of the tongue, inducing endpoint errors. We hypothesize that the spatial parameters of the error will be reported via climbing fiber inputs to the P-cells, inducing error-dependent plasticity. Thus, we will develop a task in which the tongue experiences errors, then quantify the encoding of those errors in the climbing fibers, as well as the error induced trial-to-trial changes in the simple spikes of the P-cells. Overall, our goal is to help expand the field of lingual neuroscience by developing a new NHP model in marmosets.