scholarly journals A neuroanatomically grounded optimal control model of the compensatory eye movement system

2019 ◽  
Author(s):  
P.J. Holland ◽  
T.M. Sibindi ◽  
M. Ginzburg ◽  
S. Das ◽  
K. Arkesteijn ◽  
...  

AbstractWe present a working model of the compensatory eye movement system. 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 non-linear summation 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.


2020 ◽  
Vol 123 (1) ◽  
pp. 243-258 ◽  
Author(s):  
Kristin N. Hageman ◽  
Margaret R. Chow ◽  
Dale Roberts ◽  
Charles C. Della Santina

Head rotation, translation, and tilt with respect to a gravitational field elicit reflexive eye movements that partially stabilize images of Earth-fixed objects on the retinas of humans and other vertebrates. Compared with the angular vestibulo-ocular reflex, responses to translation and tilt, collectively called the otolith-ocular reflex (OOR), are less completely characterized, typically smaller, generally disconjugate (different for the 2 eyes) and more complicated in their relationship to the natural stimuli that elicit them. We measured binocular 3-dimensional OOR responses of 6 alert normal chinchillas in darkness during whole body tilts around 16 Earth-horizontal axes and translations along 21 axes in horizontal, coronal, and sagittal planes. Ocular countertilt responses to 40-s whole body tilts about Earth-horizontal axes grew linearly with head tilt amplitude, but responses were disconjugate, with each eye’s response greatest for whole body tilts about axes near the other eye’s resting line of sight. OOR response magnitude during 1-Hz sinusoidal whole body translations along Earth-horizontal axes also grew with stimulus amplitude. Translational OOR responses were similarly disconjugate, with each eye’s response greatest for whole body translations along its resting line of sight. Responses to Earth-horizontal translation were similar to those that would be expected for tilts that would cause a similar peak deviation of the gravitoinertial acceleration (GIA) vector with respect to the head, consistent with the “perceived tilt” model of the OOR. However, that model poorly fit responses to translations along non-Earth-horizontal axes and was insufficient to explain why responses are larger for the eye toward which the GIA vector deviates. NEW & NOTEWORTHY As the first in a pair of papers on Binocular 3D Otolith-Ocular Reflexes, this paper characterizes binocular 3D eye movements in normal chinchillas during tilts and translations. The eye movement responses were used to create a data set to fully define the normal otolith-ocular reflexes in chinchillas. This data set provides the foundation to use otolith-ocular reflexes to back-project direction and magnitude of eye movement to predict tilt axis as discussed in the companion paper.



2006 ◽  
Vol 96 (5) ◽  
pp. 2819-2825 ◽  
Author(s):  
Seiji Ono ◽  
Michael J. Mustari

Smooth pursuit (SP)-related neurons in the dorsal-medial part of medial superior temporal cortex (MSTd) carry extraretinal signals that may play a role in maintenance of SP once eye velocity matches target velocity. For example, it has not been determined whether the extraretinal signals reflect volitional SP commands or proprioception. The aim of this study was to test some potential sources of extraretinal signals in MSTd pursuit neurons. We tested 40 MSTd neurons during step-ramp SP with target blink conditions to show that they carried an extraretinal signal. To examine potential contributions from eye movements that might reflect proprioceptive feedback from eye muscles, we tested MSTd neurons during rotational vestibular ocular reflex in complete darkness (VORd). Vestibular stimulation was delivered in the earth horizontal plane to elicit reflex driven smooth eye movements that matched the speed and frequency of volitional SP. We also tested VOR in the light (VORx1) and cancellation of the VOR (VORx0). Our neurons were modulated during both SP and cancellation of the VOR. In contrast, MSTd smooth pursuit neurons with extraretinal signals were not significantly modulated during VORd (sensitivity ≤ 0.10 spike/s/°/s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SP-related MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways.



1999 ◽  
Vol 81 (5) ◽  
pp. 2538-2557 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal–related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal’s head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3–1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement–related units were significantly affected by viewing distance. The viewing distance–related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)–related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance–related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal–related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR.



2012 ◽  
Vol 25 (0) ◽  
pp. 171-172
Author(s):  
Fumio Mizuno ◽  
Tomoaki Hayasaka ◽  
Takami Yamaguchi

Humans have the capability to flexibly adapt to visual stimulation, such as spatial inversion in which a person wears glasses that display images upside down for long periods of time (Ewert, 1930; Snyder and Pronko, 1952; Stratton, 1887). To investigate feasibility of extension of vision and the flexible adaptation of the human visual system with binocular rivalry, we developed a system that provides a human user with the artificial oculomotor ability to control their eyes independently for arbitrary directions, and we named the system Virtual Chameleon having to do with Chameleons (Mizuno et al., 2010, 2011). The successful users of the system were able to actively control visual axes by manipulating 3D sensors held by their both hands, to watch independent fields of view presented to the left and right eyes, and to look around as chameleons do. Although it was thought that those independent fields of view provided to the user were formed by eye movements control corresponding to pursuit movements on human, the system did not have control systems to perform saccadic movements and compensatory movements as numerous animals including human do. Fluctuations in dominance and suppression with binocular rivalry are irregular, but it is possible to bias these fluctuations by boosting the strength of one rival image over the other (Blake and Logothetis, 2002). It was assumed that visual stimuli induced by various eye movements affect predominance. Therefore, in this research, we focused on influenced of patterns of eye movements on visual perception with binocular rivalry, and implemented functions to produce saccadic movements in Virtual Chameleon.



1991 ◽  
Vol 66 (6) ◽  
pp. 2125-2140 ◽  
Author(s):  
A. M. Pastor ◽  
B. Torres ◽  
J. M. Delgado-Garcia ◽  
R. Baker

1. The discharge of antidromically identified medial rectus and abducens motoneurons was recorded in restrained unanesthesized goldfish during spontaneous eye movements and in response to vestibular and optokinetic stimulation. 2. All medial rectus and abducens motoneurons exhibited a similar discharge pattern. A burst of spikes accompanied spontaneous saccades and fast phases during vestibular and optokinetic nystagmus in the ON-direction. Firing rate decreased for the same eye movements in the OFF-direction. All units showed a steady firing rate proportional to eye position beyond their recruitment threshold. 3. Motoneuronal position (ks) and velocity (rs) sensitivity for spontaneous eye movements were calculated from the slope of the rate-position and rate-velocity linear regression lines, respectively. The averaged ks and rs values of medial rectus motoneurons were higher than those of abducens motoneurons. The differences in motoneuronal sensitivity coupled with structural variations in the lateral versus the medial rectus muscle suggest that symmetric nasal and temporal eye movements are preserved by different motor unit composition. Although the abducens nucleus consists of distinct rostral and caudal subgroups, mean ks and rs values were not significantly different between the two populations. 4. Every abducens and medial rectus motoneuron fired an intense burst of spikes during its corresponding temporal or nasal activation phase of the "eye blink." This eye movement consisted of a sequential, rather than a synergic, contraction of both vertical and horizontal extraocular muscles. The eye blink could act neither as a protective reflex nor as a goal-directed eye movement because it could not be evoked in response to sensory stimuli. We propose a role for the blink in recentering eye position. 5. Motoneuronal firing rate after ON-directed saccades decreased exponentially before reaching the sustained discharge proportional to the new eye position. Time constants of the exponential decay ranged from 50 to 300 ms. Longer time constants after the saccade were associated with backward drifts of eye position and shorter time constants with onward drifts. These postsaccadic slide signals are suggested to encode the transition of eye position to the new steady level. 6. Motoneurons modulated sinusoidally in response to sinusoidal head rotation in the dark, but for a part of the cycle they went into cutoff, dependent on their eye position recruitment threshold. Eye position (kv) and velocity (rv) sensitivity during vestibular stimulation were measured at frequencies between 1/16 and 2 Hz. Motoneuronal time constants (tau v = rv/kv) decreased on the average by 25% with the frequency of vestibular stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)



1976 ◽  
Vol 39 (4) ◽  
pp. 852-870 ◽  
Author(s):  
D. L. Robinson ◽  
R. H. Wurtz

1. In order to see whether cells in the superficial layers of the monkey superior colliculus can differentiate between real stimulus movement and self-induced stimulus movement we compared the discharge of these cells to stimulus movement in front of the stationary eye with stimulus movement generated by eye movements across a stationary stimulus. 2. Most of the cells recorded (65% of 231 cells) responded to stimulus velocities in front of the stationary eye as fast as those occurring during the peak velocity of a saccadic eye movement. Those cells that do respond usually have weak inhibitory regions and tend to have receptive fields further from fovea. 3. Move (61% of 105 cells) of the cells that did respond to rapid stimulus movement did not respond when an eye movement swept the receptive field over a stationary stimulus. 4. About half of these cells differentiated between these stimulus conditions when we used stimuli at least 1 log unit above background illumination; the remaining cells differentiated for stimuli 2 and 3 log units above background. Many cells differentiated between the two stimulus conditions over a wide range of directions of movement and the effect appears with about equal frequency in receptive fields at all distances from the fovea. 5. The differentiation is present for most cells even when the background illumination is reduced, indicating that visual factors are not the cause of the effect on these cells but may modify the response of other cells. 6. The suppression of background activity accompanying eye movements in the light is present following eye movements made in total darkness; the suppression, therefore, must result from an extraretinal signal. 4. The failure of these cells to respond to visual stimulation during eye movements is due to the same extraretinal signal that produces the suppression since a) the cells that show this suppression tend to be those that fail to respond to stimuli during eye movements, b) the time course of the suppression matches the time at which the effects of visual stimulation during an eye movement would reach the colliculus, and c) the cells which differentiate also show a decreased responsiveness to visual stimulation during the time of background suppression. While this extraretinal signal has the characteristics one would expect of a corollary discharge, proprioception as a source of the signal cannot be excluded. 8. Cells which differentiate between the two stimulus conditions usually also show an enhanced response to a visual stimulus in their receptive field when it is to be the target for a saccadic eye movement. These cells in the superior colliculus receive an extraretinal input which permits them to differentiate betweent real stimulus movements and stimulus movements resulting from the monkey's own eye movements. This differentiation would provide an uncontaminated visual movement signal and facilitate the detection of real movement in the environment...



eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Axel Lindner ◽  
Daniel Wiesen ◽  
Hans-Otto Karnath

The static magnetic field of MRI scanners can induce a magneto-hydrodynamic stimulation of the vestibular organ (MVS). In common fMRI settings, this MVS effect leads to a vestibular ocular reflex (VOR). We asked whether – beyond inducing a VOR – putting a healthy subject in a 3T MRI scanner would also alter goal-directed spatial behavior, as is known from other types of vestibular stimulation. We investigated 17 healthy volunteers, all of which exhibited a rightward VOR inside the MRI-scanner as compared to outside-MRI conditions. More importantly, when probing the distribution of overt spatial attention inside the MRI using a visual search task, subjects scanned a region of space that was significantly shifted toward the right. An additional estimate of subjective straight-ahead orientation likewise exhibited a rightward shift. Hence, putting subjects in a 3T MRI-scanner elicits MVS-induced horizontal biases of spatial orienting and exploration, which closely mimic that of stroke patients with spatial neglect.



2021 ◽  
Author(s):  
tara afra ◽  
mohammad reza salehi ◽  
Ebrahim Abiri

Abstract In this paper, a metasurface-based waveguide display equipped with an eye movement monitoring system is presented. In the suggested device, the functions of the eye movement system and AR are completely independent of each other and are designed in two separate sections at wavelengths 775 nm and 635 nm respectively. In the next part, in order to investigate the effects of the shape of the waveguide on FOV and efficiency, a multifunctional display system comprise of a single rectangular waveguide with two sensitive polarization channels are designed to operate as an AR and eye movement monitoring system simultaneously at visible and IR wavelengths respectively. In both devices, monitoring eye movements can be done over the range of -24º to 24º and the digital images are displaced in the user’s FOV based on horizontal eye positions. Although the first suggested system is heavier than one, its FOV is almost more than twice of the second system. The results indicate that metasurface-based waveguide technology can be considered as an appropriate platform for developing wearable eye movement systems.



2017 ◽  
Author(s):  
Ricky R Savjani ◽  
Elizabeth Halfen ◽  
Jung Hwan Kim ◽  
David Ress

SummaryThe superior colliculus (SC) is a layered midbrain structure involved in directing eye movements and coordinating visual attention. Electrical stimulation and neuronal recordings in the intermediate layers of monkey SC have shown a retinotopic organization for the mediation of saccadic eye-movements. However, in human SC the topography of saccades is unknown. Here, a novel experimental paradigm and highresolution (1.2-mm) functional magnetic resonance imaging methods were used to measure activity evoked by saccadic eye movements within SC. Results provide three critical observations about the topography of the human SC: (1) saccades along the superior-inferior visual axis are mapped across the medial-lateral anatomy of the SC; (2) the saccadic eye-movement representation is in register with the retinotopic organization of visual stimulation; and (3) activity evoked by saccades occurs deeper within SC than that evoked by visual stimulation. These approaches lay the foundation for studying the organization of human subcortical eye-movement mechanisms.HighlightsHigh-resolution functional MRI enabled imaging from intermediate layers of human SCSaccades along superior-inferior visual field are mapped across medial-lateral SCSaccadic eye movement maps lie deeper in SC and are in alignment with retinotopyeTOC BlurbSavjani et al. found the polar angle representation of saccadic eye movements in human SC. The topography is similar in monkey SC, is in register with the retinotopic organization evoked by visual stimulation, but lies within deeper layers. These methods enable investigation of human subcortical eye-movement organization and visual function.



1991 ◽  
Vol 3 (4) ◽  
pp. 345-350 ◽  
Author(s):  
Anne Boylan Clohessy ◽  
Michael I. Posner ◽  
Mary K. Rothbart ◽  
Shaun P. Vecera

The posterior visual spatial attention system involves a number of separable computations that allow orienting to visual locations. We have studied one of these computations, inhibition of return, in 3-, 4-, 6-, 12-, and 18--month-old infants and adults. Our results indicate that this computation develops rapidly between 3 and 6 months, in conjunction with the ability to program eye movements to specific locations. These findings demonstrate that an attention computation involving the mid-brain eye movement system develops after the third month of life. We suggest how this development might influence the infant's ability to represent and expect visual objects.



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