A comparative study of neural activity of the vermis and the lateral areas of the mouse cerebellum during a locomotion task

Abstract

Evidence gathered across various animal models suggests that in the cerebellum, sensory and motor coding integrate. I therefore aimed to characterise the activity of cerebellar vermis neurons in mice performing a task involving both motor and sensory learning. I used multi-electrode-arrays to record from populations of cerebellar neurons in head-fixed mice running in a virtual reality (VR) environment. I show that cerebellar vermis neurons modulate their activity according to the speed of locomotion, having either a positive or negative relationship with increasing speed or responding maximally to a given speed. Moreover, some neurons tune their firing rate to the stepping frequency; this relationship becomes more distinct with increasing speed. I then demonstrate that a subset of neurons can detect the initiation and the termination of locomotion. I also show that a minority of neurons display preferred responses to either clockwise or counter-clockwise yaw direction, suggesting that some neurons receive lateralised proprioceptive information. Finally, I compare the cerebellar vermis neural responses with the activity of neurons recorded from the lateral cerebellum of mice performing the same behavioural task. I show that neurons from both cerebellar areas are able to encode locomotion-related kinematic parameters, but the differences in the way they do so is indicative of their efferent and afferent connections with the rest of the nervous system. This work is the first to characterize a population of lateral cerebellum neurons in a VR environment, providing new data for sensorimotor integration and navigation models. In the future, population recordings, further characterization of the functional connectivity of the lateral cerebellum, and targeted behavioural tasks can improve understanding of how the different areas of the cerebellum work together to achieve sensorimotor control and learning.