A Computational System-Level Model of Oculomotor Pathways Accounting for the Representation of Eye Biomechanics in the Cerebellar Vermis

Christian Darlot,Mohammad Mehdi Ebadzadeh,Zahra Ghorrati,Armin Salimi-Badr,Mitra Asadi-Eydivand

doi:10.1109/access.2020.3002378

Abstract

In this paper a comprehensive system-level computational model of oculomotor pathways is presented. This model shows the necessity of embedding internal models of muscles biomechanics in the cerebellar Vermis to realize fast saccadic eye movements based on predicting the changes in muscles lengths. First, the eye biomechanics are described by nonlinear equations during “slow” and “fast” movements. Afterward, by analyzing these equations, a computational model, is deduced. Furthermore, each part of this model is interpreted as a possible function of an element in the oculomotor pathways based on physiological and anatomical pieces of evidence. In this model, two internal feedback loops compensate two types of error: 1- error between desired and estimated values of eye position, calculated by Superior Colliculus, and 2- error between desired and estimated torque, calculated by Cerebellar pathways. Simulations of this circuit produce signals similar to the actual neuronal activities in the corresponding sites of the oculomotor pathways during saccades. Effects of bilateral lesions of Fastigial nuclei, Vermis, Prepositus Hypoglossi, the stimulation of Omni-Pause Neuron and Superior Colliculus are studied. Furthermore, the model ability in performing smooth pursuit eye movements is investigated. Finally, the “main sequence” is reproduced. This model is the first one to derive both the cerebellar function and the bilateral connectivity of the oculomotor pathways from calculations based on physical hypotheses. The proposed model is useful to better understand computational functions of different parts of the oculomotor pathways, and also using in robotics application for controlling fast movement inspired by the brain.

Highlights

During recent decades, many experimental and theoretical studies have been performed to comprehend the principles of motor control and better understand motor diseases [1]–[6]
PHYSIOLOGICAL AND ANATOMICAL REVIEW The entire oculomotor system is composed of two parts: 1) The biomechanical system, consisting of the eye, the muscles, and the connective tissues; 2) The neural motor circuit which prepares the motor commands sent to the muscles, and is composed of functionally articulated sub-circuits exchanging messages encoded in neural signals
The signals issued from the motor Cerebral Cortex and the Superior Colliculus are complemented by signals, computed in the Cerebellum according to the estimated state of the muscles, and sent from the contralateral Fastigial nucleus to the Excitatory Burst Neurons’’ (EBNs) and Nucleus Reticularis Tegmenti Pontis (NRTP)

Summary

INTRODUCTION

Many experimental and theoretical studies have been performed to comprehend the principles of motor control and better understand motor diseases [1]–[6]. Signals encoding estimates of angular velocity and position, recorded in the Prepositus Hypoglossi (PH) nucleus, reach the Superior Colliculus (SC) and the Cerebellum [37], and signals encoding predicted muscle lengths, recorded in the Vermis, reach the Fastigial nucleus By means of these inner signals, motor commands can be calculated in a closed loop manner based on internal estimated feedback without delay, instead of using real sensory feedback received by delay [38].

PHYSIOLOGICAL AND ANATOMICAL REVIEW

DISCUSSION

CONCLUSION