Direct causality between single-Purkinje cell activities and motor learning revealed by a cerebellum-machine interface utilizing VOR adaptation paradigm.

A cerebellum-machine interface (CMI) was developed to test direct causality between single-unit cerebellar Purkinje cell activities and motor learning. The CMI converts Purkinje cell simple spike firing rates into a pulse width modulation signal that drives a single-joint robot arm. The CMI has no adaptive capability, thus any changes observed in the robot arm motion can be attributed directly to changes in the Purkinje cell's firing activities. We employed a vestibuloocular reflex (VOR) adaptation paradigm in goldfish as an example of motor learning where desired motion and control error signal of the robot arm were given to the fish as its head rotation and retinal slip, respectively. It is demonstrated that the control error of the robot arm decreased gradually, but not monotonically and in many cases only in one direction. This is the first direct evidence that a single Purkinje cell is capable of adaptive motor control. The results also suggest that a single Purkinje cell can be responsible for directional selective VOR motor learning previously reported in goldfish by Yoshikawa et al. (Conf Proc IEEE Eng Med Biol Soc 1:478-481, 2004) and monkeys by Hirata et al. (J Neurophysiol 85(5):2267-2288, 2002).