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

Abstract

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.

A generative learning model for saccade adaptation

“…On a neurophysiological level, the small systematic bias that gives rise to the drift of the baseline may originate from the dynamics of the responses in the neuronal substrates involved with saccade adaptation ([55–60], R. Shadmehr, personal communication , July 12, 2018). It is also possible that the fast-pacing used in our paradigm exacerbates effects that generate a small and negative bias parameter, m , which appeared to onset already at the pre-adaptation block.…”

“…We believe that the presence of a systematically varying disturbance enables a further decomposition of the implicit component of adaptation, perhaps into a primary one, that attempts to mitigate the end-point discrepancy regardless of self-correlations in the disturbance, and a second one that attempts to extract (and use) such correlations. It remains an open question how these putative subprocesses may map on distinct or overlapping anatomical structures, such as cerebellar cortices, deep cerebellar nuclei and extracerebellar structures [55,57,59,60,64,76–80].…”

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

“…We used the same control loop described in (15, 16). The control loop is split into three components (see Fig 1a).…”

“…In control theory, a common assumption is that a rate code might suffice. For example, recent models used a continuous rate-based representation of neural activity (16, 27) to reproduce the PC population responses that try to optimize movement kinematics. However, it has been proposed that cerebellar cortex relies on millisecond spike precision of PCs, not on individual firing rates, to convey to the nucleus when to stop a movement (28).…”

“…Notably, the absence of cerebellar contribution does not eliminate the ability to make saccades, but significantly affects the vigor and accuracy of the movements (14). Hence, the control system can be comprised of an imprecise base controller connected with the cerebellum, which can act as an adaptive controller that fine tunes the sluggish base control policy (15,16). Several computational models focused on the cerebellum involvement in saccadic control (15,(17)(18)(19) and adaptation (20,21) and accounted for residual behavioral response following cerebellar lesions (22,23).…”