A Neuroanatomically Grounded Optimal Control Model of the Compensatory Eye Movement System in Mice

Peter Holland, Tafadzwa Sibindi, S Ginzburg, Suman Das, K Arkesteijn, Maarten Frens, Opher Donchin

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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.

Original languageEnglish
Article number13
Pages (from-to)1-19
Number of pages19
JournalFrontiers in Systems Neuroscience
Volume14
DOIs
Publication statusPublished - 2021

Bibliographical note

Funding Information:
Parts are based on chapters of the theses of TS (Sibindi, 2015) and SD (Das, 2017). Funding. This research was supported by the C7 Marie Curie ITN initiative (TS, PH, SD), TC2N Interreg Grant (OD, MF), the ABC Robotics Initiative (OD), and a Post-Doctoral Fellowship from the Kreitman School for Advanced Studies at BGU (PH).

Funding Information:
This research was supported by the C7 Marie Curie ITN initiative (TS, PH, SD), TC2N Interreg Grant (OD, MF),

Publisher Copyright:
© Copyright © 2020 Holland, Sibindi, Ginzburg, Das, Arkesteijn, Frens and Donchin.

Research programs

  • EMC OR-01

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