Abstract

We present a working model of the compensatory eye movement system in mice. We challenge the model with a data set of eye movements in mice (n =34) recorded in 4 different sinusoidal stimulus conditions with 36 different combinations of frequency (0.1–3.2 Hz) and amplitude (0.5–8°) in each condition. The conditions included vestibular stimulation in the dark (vestibular-ocular reflex, VOR), optokinetic stimulation (optokinetic reflex, OKR), and two combined visual/vestibular conditions (the visual-vestibular ocular reflex, vVOR, and visual suppression of the VOR, sVOR). The model successfully reproduced the eye movements in all conditions, except for minor failures to predict phase when gain was very low. Most importantly, it could explain the interaction of VOR and OKR when the two reflexes are activated simultaneously during vVOR stimulation. In addition to our own data, we also reproduced the behavior of the compensatory eye movement system found in the existing literature. These include its response to sum-of-sines stimuli, its response after lesions of the nucleus prepositus hypoglossi or the flocculus, characteristics of VOR adaptation, and characteristics of drift in the dark. Our model is based on ideas of state prediction and forward modeling that have been widely used in the study of motor control. However, it represents one of the first quantitative efforts to simulate the full range of behaviors of a specific system. The model has two separate processing loops, one for vestibular stimulation and one for visual stimulation. Importantly, state prediction in the visual processing loop depends on a forward model of residual retinal slip after vestibular processing. In addition, we hypothesize that adaptation in the system is primarily adaptation of this model. In other words, VOR adaptation happens primarily in the OKR loop.

Highlights

  • Compensatory eye movement (CEM) is a general term for several reflexes whose goal is to maintain a stable image on the retina during movements of the head by moving the eyes in the opposite direction (Delgado-García, 2000)

  • The behavioral data that we present are in agreement with the values that have been previously published for the C57BL/6 mouse strain (Stahl et al, 2000; Faulstich et al, 2004; van Alphen et al, 2010; Schonewille et al, 2011)

  • The vestibulo-ocular reflex (VOR) (Figure 3) in the dark responded to high frequency stimulation, and the optokinetic reflex (OKR) (Figure 4) was mainly active in response to low velocity stimuli

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Summary

Introduction

Compensatory eye movement (CEM) is a general term for several reflexes whose goal is to maintain a stable image on the retina during movements of the head by moving the eyes in the opposite direction (Delgado-García, 2000). In other words, these reflexes serve to reduce retinal slip (movement of the visual image across the retina). The two reflexes have roughly complementary properties: the OKR performs well in low velocities and the VOR works well at high frequencies The existence of these reflexes allows accurate compensation of retinal slip velocities experienced in normal behavior. The model must function in the presence of motor and sensory noise as well as including realistic delays involved in visual sensation

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