Dual STDP processes at Purkinje cells contribute to distinct improvements in accuracy and speed of saccadic eye movements

Saccadic eye-movements play a crucial role in visuo-motor control by allowing rapid foveation onto new targets. However, the neural processes governing saccades adaptation are not fully understood. Saccades, due to the short-time of execution (20-100 ms) and the absence of sensory information for online feedback control, must be controlled in a ballistic manner. Incomplete measurements of the movement trajectory, such as the visual end-point error, are supposedly used to form internal predictions about the movement kinematics resulting in predictive control. In order to characterize the synaptic and neural circuit mechanisms underlying predictive saccadic control, we have reconstructed the saccadic system in a digital controller embedding a spiking neural network of the cerebellum with spike timing-dependent plasticity (STDP) rules driving parallel fiber - Purkinje cell long-term potentiation and depression (LTP and LTD). This model implements a control policy based on a dual plasticity mechanism, resulting in the identification of the roles of LTP and LTD in optimizing saccade movement control: it turns out that LTD regulates the accuracy and LTP the speed (vigor) of the ballistic eye movement. The control policy also required cerebellar PCs to be divided into two subpopulations, characterized by burst or pause responses. To our knowledge, this is the first model that explains in mechanistic terms the accuracy and vigor regulation of ballistic eye movements in forward mode exploiting spike-timing to regulate firing in different populations of the neuronal network. This elementary model of saccades could be extended and applied to other more complex cases in which single jerks are concatenated to compose articulated and coordinated movements. Author summary It has been suggested that the cerebellum plays a crucial role in oculomotor adaptation. Computationally, the cerebellum is described as a supervised learner whose activity can be adjusted by synaptic changes proportional to the amount of mismatch between expected and actual movements outcomes (sensorimotor-errors). However, the spike-timing-dependent-plasticity (STDP) underlying adaptation has been so far modeled in behaviors where the error is continuously available as tracking-error. Such models depend on detailed tracking-errors to improve movement quality. We asked if the cerebellum can maintain good motor control even if the error is not completely available? This is important considering that error-dependent-STDP is only a subset among a family of STDP processes in the cerebellum. Moreover, even the physiological signals that were generally thought to carry sensorimotor-errors (called complex-spikes) are shown to encode multiple types of information regarding the movement. In this context, we characterize the role of cerebellar STDPs in saccade control, where the error information is constrained because of sensory suppression. We show that even in the absence of detailed error, the cerebellum can leverage two of its STDPs to increase movement quality. Hence, we emphasize the need to go beyond error-centric view to understand how the cerebellum improves motor behavior.