Corollary discharge provides accurate eye position information to the oculomotor system

Science ◽  
1983 ◽  
Vol 221 (4616) ◽  
pp. 1193-1195 ◽  
Author(s):  
B. Guthrie ◽  
J. Porter ◽  
D. Sparks
Keyword(s):  
Oculomotor System ◽  
Corollary Discharge ◽  
Eye Position ◽  
Position Information

Implications of rotational kinematics for the oculomotor system in three dimensions

1987 ◽  
Vol 58 (4) ◽  
pp. 832-849 ◽  
Author(s):  
D. Tweed ◽  
T. Vilis
Keyword(s):  
Three Dimensional ◽  
Oculomotor System ◽  
Three Dimensions ◽  
Eye Position ◽  
Head Velocity ◽  
Listing’S Law ◽  
Indirect Path ◽  
Dimensional Models ◽  
Three Dimensional Models ◽  
Eye Velocity

1. This paper develops three-dimensional models for the vestibuloocular reflex (VOR) and the internal feedback loop of the saccadic system. The models differ qualitatively from previous, one-dimensional versions, because the commutative algebra used in previous models does not apply to the three-dimensional rotations of the eye. 2. The hypothesis that eye position signals are generated by an eye velocity integrator in the indirect path of the VOR must be rejected because in three dimensions the integral of angular velocity does not specify angular position. Computer simulations using eye velocity integrators show large, cumulative gaze errors and post-VOR drift. We describe a simple velocity to position transformation that works in three dimensions. 3. In the feedback control of saccades, eye position error is not the vector difference between actual and desired eye positions. Subtractive feedback models must continuously adjust the axis of rotation throughout a saccade, and they generate meandering, dysmetric gaze saccades. We describe a multiplicative feedback system that solves these problems and generates fixed-axis saccades that accord with Listing's law. 4. We show that Listing's law requires that most saccades have their axes out of Listing's plane. A corollary is that if three pools of short-lead burst neurons code the eye velocity command during saccades, the three pools are not yoked, but function independently during visually triggered saccades. 5. In our three-dimensional models, we represent eye position using four-component rotational operators called quaternions. This is not the only algebraic system for describing rotations, but it is the one that best fits the needs of the oculomotor system, and it yields much simpler models than do rotation matrix or other representations. 6. Quaternion models predict that eye position is represented on four channels in the oculomotor system: three for the vector components of eye position and one inversely related to gaze eccentricity and torsion. 7. Many testable predictions made by quaternion models also turn up in models based on other mathematics. These predictions are therefore more fundamental than the specific models that generate them. Among these predictions are 1) to compute eye position in the indirect path of the VOR, eye or head velocity signals are multiplied by eye position feedback and then integrated; consequently 2) eye position signals and eye or head velocity signals converge on vestibular neurons, and their interaction is multiplicative.(ABSTRACT TRUNCATED AT 400 WORDS)

Oculomotor Control of Primary Eye Position Discriminates Between Translation and Tilt

1999 ◽  
Vol 81 (1) ◽  
pp. 394-398 ◽  
Author(s):  
Bernhard J. M. Hess ◽  
Dora E. Angelaki
Keyword(s):  
Dynamic Control ◽  
Linear Acceleration ◽  
Oculomotor System ◽  
Oculomotor Control ◽  
Eye Position ◽  
Axis Orientation ◽  
Fast Phase ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Head Rotations

Hess, Bernhard J. M. and Dora E. Angelaki. Oculomotor control of primary eye position discriminates between translation and tilt. J. Neurophysiol. 81: 394–398, 1999. We have previously shown that fast phase axis orientation and primary eye position in rhesus monkeys are dynamically controlled by otolith signals during head rotations that involve a reorientation of the head relative to gravity. Because of the inherent ambiguity associated with primary otolith afferent coding of linear accelerations during head translation and tilts, a similar organization might also underlie the vestibulo-ocular reflex (VOR) during translation. The ability of the oculomotor system to correctly distinguish translational accelerations from gravity in the dynamic control of primary eye position has been investigated here by comparing the eye movements elicited by sinusoidal lateral and fore-aft oscillations (0.5 Hz ± 40 cm, equivalent to ± 0.4 g) with those during yaw rotations (180°/s) about a vertically tilted axis (23.6°). We found a significant modulation of primary eye position as a function of linear acceleration (gravity) during rotation but not during lateral and fore-aft translation. This modulation was enhanced during the initial phase of rotation when there was concomitant semicircular canal input. These findings suggest that control of primary eye position and fast phase axis orientation in the VOR are based on central vestibular mechanisms that discriminate between gravity and translational head acceleration.

Motor Dynamics Encoding in Cat Cerebellar Flocculus Middle Zone During Optokinetic Eye Movements

1999 ◽  
Vol 82 (5) ◽  
pp. 2235-2248 ◽  
Author(s):  
Toshihiro Kitama ◽  
Tomohiro Omata ◽  
Akihito Mizukoshi ◽  
Takehiko Ueno ◽  
Yu Sato
Keyword(s):  
Time Course ◽  
Inverse Dynamics ◽  
Coefficient Of Determination ◽  
Eye Position ◽  
Middle Zone ◽  
Forward Selection ◽  
Optokinetic Response ◽  
Position Information ◽  
Stimulus Velocity ◽  
Cerebellar Flocculus

We investigated the relationship between eye movement and simple-spike (SS) frequency of Purkinje cells in the cerebellar flocculus middle zone during the optokinetic response (OKR) in alert cats. The OKR was elicited by a sequence of a constant-speed visual pattern movement in one direction for 1 s and then in the opposite direction for 1 s. Quick-phase-free trials were selected. Sixty-six cells had direction-selective complex spike (CS) activity that was modulated during horizontal (preferring contraversive) but not vertical stimuli. The SS activity was modulated during horizontal OKR, preferring ipsiversive stimuli. Forty-one cells had well-modulated activity and were suitable for the regression model. In these cells, an inverse dynamics approach was applied, and the time course of the SS rate was reconstructed, with mean coefficient of determination 0.76, by a linear weighted superposition of the eye acceleration (mean coefficient, 0.056 spikes/s per deg/s2), velocity (5.10 spikes/s per deg/s), position (−2.40 spikes/s per deg), and constant (mean 34.3 spikes/s) terms, using a time delay (mean 11 ms) from the unit response to the eye response. The velocity and acceleration terms contributed to the increase in the reconstructed SS rates during ipsilateral movements, whereas the position term contributed during contralateral movements. The standard regression coefficient analyses revealed that the contribution of the velocity term (mean coefficient 0.81) was predominant over the acceleration (0.03) and position (−0.17) terms. Forward selection analysis revealed three cell types: Velocity-Position-Acceleration type ( n = 27): velocity, position, and acceleration terms are significant ( P < 0.05); Velocity-Position type ( n = 12): velocity and position terms are significant; and Velocity-Acceleration type ( n = 2): velocity and acceleration terms are significant. Using the set of coefficients obtained by regression of the response to a 5 deg/s stimulus velocity, the SS rates during higher (10, 20, and 40 deg/s) stimulus velocities were successfully reconstructed, suggesting generality of the model. The eye-position information encoded in the SS firing during the OKR was relative but not absolute in the sense that the magnitude of the position shift from the initial eye position (0 deg/s velocity) contributed to firing rate changes, but the initial eye position did not. It is concluded that 1) the SS firing frequency in the cat middle zone encodes the velocity and acceleration information for counteracting the viscosity and inertia forces respectively, during short-duration horizontal OKR and 2) the apparent position information encoded in the SS firing is not appropriate for counteracting the elastic force during the OKR.

Human Oculomotor System Accounts for 3-D Eye Orientation in the Visual-Motor Transformation for Saccades

1998 ◽  
Vol 80 (5) ◽  
pp. 2274-2294 ◽  
Author(s):  
Eliana M. Klier ◽  
J. Douglas Crawford
Keyword(s):  
Reference Frame ◽  
Oculomotor System ◽  
Gaze Direction ◽  
Eye Position ◽  
Look Up Table ◽  
Listing's Law ◽  
Listing’S Law ◽  
Reference Frame Transformation ◽  
Visual Motor ◽  
Frame Transformation

Klier, Eliana M. and J. Douglas Crawford. Human oculomotor system accounts for 3-D eye orientation in the visual-motor transformation for saccades. J. Neurophysiol. 80: 2274–2294, 1998. A recent theoretical investigation has demonstrated that three-dimensional (3-D) eye position dependencies in the geometry of retinal stimulation must be accounted for neurally (i.e., in a visuomotor reference frame transformation) if saccades are to be both accurate and obey Listing's law from all initial eye positions. Our goal was to determine whether the human saccade generator correctly implements this eye-to-head reference frame transformation (RFT), or if it approximates this function with a visuomotor look-up table (LT). Six head-fixed subjects participated in three experiments in complete darkness. We recorded 60° horizontal saccades between five parallel pairs of lights, over a vertical range of ±40° ( experiment 1), and 30° radial saccades from a central target, with the head upright or tilted 45° clockwise/counterclockwise to induce torsional ocular counterroll, under both binocular and monocular viewing conditions ( experiments 2 and 3). 3-D eye orientation and oculocentric target direction (i.e., retinal error) were computed from search coil signals in the right eye. Experiment 1: as predicted, retinal error was a nontrivial function of both target displacement in space and 3-D eye orientation (e.g., horizontally displaced targets could induce horizontal or oblique retinal errors, depending on eye position). These data were input to a 3-D visuomotor LT model, which implemented Listing's law, but predicted position-dependent errors in final gaze direction of up to 19.8°. Actual saccades obeyed Listing's law but did not show the predicted pattern of inaccuracies in final gaze direction, i.e., the slope of actual error, as a function of predicted error, was only −0.01 ± 0.14 (compared with 0 for RFT model and 1.0 for LT model), suggesting near-perfect compensation for eye position. Experiments 2 and 3: actual directional errors from initial torsional eye positions were only a fraction of those predicted by the LT model (e.g., 32% for clockwise and 33% for counterclockwise counterroll during binocular viewing). Furthermore, any residual errors were immediately reduced when visual feedback was provided during saccades. Thus, other than sporadic miscalibrations for torsion, saccades were accurate from all 3-D eye positions. We conclude that 1) the hypothesis of a visuomotor look-up table for saccades fails to account even for saccades made directly toward visual targets, but rather, 2) the oculomotor system takes 3-D eye orientation into account in a visuomotor reference frame transformation. This transformation is probably implemented physiologically between retinotopically organized saccade centers (in cortex and superior colliculus) and the brain stem burst generator.

Postsaccadic eye position contributes to oculomotor error estimation in saccadic adaptation

2019 ◽  
Vol 122 (5) ◽  
pp. 1909-1917
Author(s):  
Svenja Gremmler ◽  
Markus Lappe
Keyword(s):  
Visual Feedback ◽  
Eye Position ◽  
Time Interval ◽  
Proprioceptive Information ◽  
Experimental Conditions ◽  
Position Information ◽  
Saccadic Adaptation ◽  
Position Signal ◽  
Motor Error ◽  
Saccade Control

We investigated whether the proprioceptive eye position signal after the execution of a saccadic eye movement is used to estimate the accuracy of the movement. If so, saccadic adaptation, the mechanism that maintains saccade accuracy, could use this signal in a similar way as it uses visual feedback after the saccade. To manipulate the availability of the proprioceptive eye position signal we utilized the finding that proprioceptive eye position information builds up gradually after a saccade over a time interval comparable to typical saccade latencies. We confined the retention time of gaze at the saccade landing point by asking participants to make fast return saccades to the fixation point that preempt the usability of proprioceptive eye position signals. In five experimental conditions we measured the influence of the visual and proprioceptive feedback, together and separately, on the development of adaptation. We found that the adaptation of the previously shortened saccades in the case of visual feedback being unavailable after the saccade was significantly weaker when the use of proprioceptive eye position information was impaired by fast return saccades. We conclude that adaptation can be driven by proprioceptive eye position feedback. NEW & NOTEWORTHY We show that proprioceptive eye position information is used after a saccade to estimate motor error and adapt saccade control. Previous studies on saccadic adaptation focused on visual feedback about saccade accuracy. A multimodal error signal combining visual and proprioceptive information is likely more robust. Moreover, combining proprioceptive and visual measures of saccade performance can be helpful to keep vision, proprioception, and motor control in alignment and produce a coherent representation of space.

Inflow as a source of extraretinal eye position information

1972 ◽  
Vol 12 (2) ◽  
pp. 221-IN7 ◽  
Author(s):  
Alexander A. Skavenski
Keyword(s):  
Eye Position ◽  
Position Information

Does the world rock when the eyes roll?

2000 ◽  
Vol 59 (2) ◽  
pp. 89-101 ◽  
Author(s):  
Fred W. Mast
Keyword(s):  
Inertial Force ◽  
Neural Mechanism ◽  
Visual Orientation ◽  
Eye Position ◽  
Position Information ◽  
Reference Information ◽  
Ocular Counterroll ◽  
Short Line Segment ◽  
Visual Vertical ◽  
The Brain

When the head is inclined sideways, the eyes are counter-rotated with respect to the head (ocular-counterroll, OCR). In man, the gain of OCR in static body tilts is limited to about 10% of the angle of roll tilt, which suggests that its function is vestigial. However, it is still unclear how the residual OCR is related to the perceived orientation of visual stimuli. Wade and Curthoys (1997) claim that the brain does not “take into account” the OCR, so that the eye position directly interferes with perception of visual orientation. Alternately, it has been argued that OCR is partly compensated by an extraretinal eye-position information such as, e.g., an efference copy ( Haustein, 1992 ; Haustein & Mittelstaedt, 1990 ). The two experiments reported in this study are targeted towards critically examining this inter-relation between OCR and perceived visual orientation. The latter was assessed via the subjective visual vertical, SVV, which is determined when a subject judges the orientation of an indicator (e.g., a short line segment) as apparently vertical. The OCR was measured by using a video-oculographic system. In Experiment 1, a human centrifuge was used to test the effect of an increase of the gravito-inertial force (GIF) on SVV and OCR. Experiment 2 was inspired by the fact that OCR can also be elicited during “barbecue rotation”. Again, it was the aim to compare OCR and SVV in different body positions, such as pure roll and barbecue rotated tilts. The present study provides convincing experimental evidence that SVV is widely uninfluenced by the course of OCR. Increasing the GIF in Experiment 1 had a divergent effect on SVV and OCR; the gain of OCR increases whereas the SVV changed differently, at obtuse tilt angles even in the opposite direction. OCR and SVV were again found to dissociate in Experiment 2, which emphasizes the fact that the SVV and OCR are not controlled by the same neural mechanism, but rather use different spatial reference information.

scholarly journals Expansion of Visual Space During Optokinetic Afternystagmus (OKAN)

2008 ◽  
Vol 99 (5) ◽  
pp. 2470-2478 ◽  
Author(s):  
André Kaminiarz ◽  
Bart Krekelberg ◽  
Frank Bremmer
Keyword(s):  
Eye Movements ◽  
Visual Space ◽  
Eye Position ◽  
Control Mechanisms ◽  
Position Information ◽  
Fast Phase ◽  
Optokinetic Afternystagmus ◽  
Perceptual Stability ◽  
Voluntary Eye Movements ◽  
The Brain

The mechanisms underlying visual perceptual stability are usually investigated using voluntary eye movements. In such studies, errors in perceptual stability during saccades and pursuit are commonly interpreted as mismatches between actual eye position and eye-position signals in the brain. The generality of this interpretation could in principle be tested by investigating spatial localization during reflexive eye movements whose kinematics are very similar to those of voluntary eye movements. Accordingly, in this study, we determined mislocalization of flashed visual targets during optokinetic afternystagmus (OKAN). These eye movements are quite unique in that they occur in complete darkness and are generated by subcortical control mechanisms. We found that during horizontal OKAN slow phases, subjects mislocalize targets away from the fovea in the horizontal direction. This corresponds to a perceived expansion of visual space and is unlike mislocalization found for any other voluntary or reflexive eye movement. Around the OKAN fast phases, we found a bias in the direction of the fast phase prior to its onset and opposite to the fast-phase direction thereafter. Such a biphasic modulation has also been reported in the temporal vicinity of saccades and during optokinetic nystagmus (OKN). A direct comparison, however, showed that the modulation during OKAN was much larger and occurred earlier relative to fast-phase onset than during OKN. A simple mismatch between the current eye position and the eye-position signal in the brain is unlikely to explain such disparate results across similar eye movements. Instead, these data support the view that mislocalization arises from errors in eye-centered position information.

Eye position effects in saccadic adaptation

2011 ◽  
Vol 106 (5) ◽  
pp. 2536-2545 ◽  
Author(s):  
Katharina Havermann ◽  
Eckart Zimmermann ◽  
Markus Lappe
Keyword(s):  
Eye Movements ◽  
Visual Space ◽  
Initial Position ◽  
Head Movements ◽  
Eye Position ◽  
Saccade Amplitude ◽  
Position Effects ◽  
Position Information ◽  
Saccadic Adaptation ◽  
Visual Error

Saccades are used by the visual system to explore visual space with the high accuracy of the fovea. The visual error after the saccade is used to adapt the control of subsequent eye movements of the same amplitude and direction in order to keep saccades accurate. Saccadic adaptation is thus specific to saccade amplitude and direction. In the present study we show that saccadic adaptation is also specific to the initial position of the eye in the orbit. This is useful, because saccades are normally accompanied by head movements and the control of combined head and eye movements depends on eye position. Many parts of the saccadic system contain eye position information. Using the intrasaccadic target step paradigm, we adaptively reduced the amplitude of reactive saccades to a suddenly appearing target at a selective position of the eyes in the orbitae and tested the resulting amplitude changes for the same saccade vector at other starting positions. For central adaptation positions the saccade amplitude reduction transferred completely to eccentric starting positions. However, for adaptation at eccentric starting positions, there was a reduced transfer to saccades from central starting positions or from eccentric starting positions in the opposite hemifield. Thus eye position information modifies the transfer of saccadic amplitude changes in the adaptation of reactive saccades. A gain field mechanism may explain the eye position dependence found.

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