Dynamic changes in the cerebellar-interpositus/red-nucleus-motoneuron pathway during motor learning

Abstract

Understanding the role played by the cerebellum in the genesis and control of learned motor responses requires a precise knowledge of interdependent relationships between kinetic neural commands and the performance (kinematics) of the acquired movements. The eyelid motor system is a useful model for studying how simple motor responses are generated and performed. Here, we recorded the activity of interpositus, red nucleus, and/or facial motor neurons during classical eyeblink conditioning, using a delay paradigm. Experiments were carried out in behaving cats, and in conscious wild-type and (Purkinje cell devoid) Lurcher mice. Kinetic variables were determined by recording the firing activities of identified neurons at the mentioned nuclei, whilst kinematic variables were selected from the electromyographic activity of the orbicularis oculi muscle and/or from eyelid position recorded during the conditioned-stimulus/ unconditioned-stimulus interval. Whereas motoneurons encoded eyelid kinematics for acquired eyelid responses, interpositus, and red nucleus neurons did not directly encode eyelid performance, and the dynamic association between their neuronal activities was barely significant (from moderate to weak correlation, nonlinear coupling with high asymmetry, and neural firing activities that always lagged the beginning of the conditioned response). Nevertheless, interpositus and red nucleus neurons seem to play a modulating role in the dynamic control of this type of learned motor response, and present interesting adaptive properties in Lurcher mice. The analytical procedures proposed here could be very helpful in defining the functional state corresponding to each stage across the acquisition of new motor and cognitive abilities.