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 endpoint 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 regulating the overall quality of saccade kinematics: it turns out that LTD increases the accuracy by decreasing visual error and LTP increases the peak speed. 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 visual error and peak speed 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.

Rotational dynamics in motor cortex are consistent with a feedback controller.

Recent studies have identified rotational dynamics in motor cortex (MC), which many assume arise from intrinsic connections in MC. However, behavioral and neurophysiological studies suggest that MC behaves like a feedback controller where continuous sensory feedback and interactions with other brain areas contribute substantially to MC processing. We investigated these apparently conflicting theories by building recurrent neural networks that controlled a model arm and received sensory feedback from the limb. Networks were trained to counteract perturbations to the limb and to reach toward spatial targets. Network activities and sensory feedback signals to the network exhibited rotational structure even when the recurrent connections were removed. Furthermore, neural recordings in monkeys performing similar tasks also exhibited rotational structure not only in MC but also in somatosensory cortex. Our results argue that rotational structure may also reflect dynamics throughout the voluntary motor system involved in online control of motor actions.

Cerebellar adaptive mechanisms explain the optimal control of saccadic eye movements.

Cerebellar synaptic plasticity is vital for adaptability and fine tuning of goal-directed movements. The perceived sensory errors between desired and actual movement outcomes are commonly considered to induce plasticity in the cerebellar synapses, with an objective to improve desirability of the executed movements. In rapid goal-directed eye movements called saccades, the only available sensory feedback is the direction of reaching error information received only at end of the movement. Moreover, this sensory error dependent plasticity can only improve the accuracy of the movements, while ignoring other essential characteristics such as reaching in minimum-time. In this work we propose a rate based, cerebellum inspired adaptive filter model to address refinement of both accuracy and movement-time of saccades. We use optimal control approach in conjunction with information constraints posed by the cerebellum to derive bio-plausible supervised plasticity rules. We implement and validate this bio-inspired scheme on a humanoid robot. We found out that, separate plasticity mechanisms in the model cerebellum separately control accuracy and movement-time. These plasticity mechanisms ensure that optimal saccades are produced by just receiving the direction of end reaching error as an evaluative signal. Furthermore, the model emulates encoding in the cerebellum of movement kinematics as observed in biological experiments.

Modeling the Encoding of Saccade Kinematic Metrics in the Purkinje Cell Layer of the Cerebellar Vermis.

Recent electrophysiological observations related to saccadic eye movements in rhesus monkeys, suggest a prediction of the sensory consequences of movement in the Purkinje cell layer of the cerebellar oculomotor vermis (OMV). A definite encoding of real-time motion of the eye has been observed in simple-spike responses of the combined burst-pause Purkinje cell populations, organized based upon their complex-spike directional tuning. However, the underlying control mechanisms that could lead to such action encoding are still unclear. We propose a saccade control model, with emphasis on the structure of the OMV and its interaction with the extra-cerebellar components. In the simulated bilateral organization of the OMV, each caudal fastigial nucleus is arranged to receive incoming projections from combined burst-pause Purkinje cell populations. The OMV, through the caudal fastigial nuclei, interacts with the brainstem to provide adaptive saccade gain corrections that minimize the visual error in reaching a given target location. The simulation results corroborate the experimental Purkinje cell population activity patterns and their relation with saccade kinematic metrics. The Purkinje layer activity that emerges from the proposed organization, precisely predicted the speed of the eye at different target eccentricities. Simulated granular layer activity suggests no separate dynamics with respect to shaping the bilateral Purkine layer activity. We further examine the validity of the simulated OMV in maintaining the accuracy of saccadic eye movements in the presence of signal dependent variabilities, that can occur in extra-cerebellar pathways.