Listing's Plane Research Articles

Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus.

The rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) contains burst neurons whose activity precedes rapid eye movements with a vertical and/or torsional component. To ascertain their causal role in the generation of conjugate eye movements, we placed uni- and bilateral kainic acid lesions in that region. Unilateral inactivation of the riMLF leads to a loss of all rapid eye movements with an ipsitorsional component (ipsitorsional is defined as movement of the upper pole of the ipsilateral eye in a temporal direction). Vertical eye movements are impaired in an asymmetric way, with downward movements slowed and upward movements little affected. Listing's plane is shifted in the contratorsional direction, i.e., we find a constant torsional offset for all eye positions. With bilateral lesions one observes a total loss of all vertical and torsional eye movements, while Listing's plane retains its shape and position. These results show that burst neurons in the riMLF play a decisive role in generating rapid eye movements with a vertical and torsional component.

An alternative three-dimensional interpretation of Hering's equal-innervation law for version and vergence eye movements

In the context of Hering's equal-innervation law, this paper discusses the problem of how the three-dimensional positions of the two eyes, each expressed by a rotation vector, can be separated into contributions of the version and vergence system. As proposed by Van Rijn and Van den Berg [(1993) Vision Research, 33, 691–708], this can be done by taking the sum and difference of the position rotation vectors of each eye. In our alternative procedure the vergence signal is defined as the rotation which transforms the left eye position into the right eye position and the version signal is the common factor in both eye positions that remains after removing the vergence signal. The version and vergence contributions, defined in this way, can be interpreted straightforwardly as rotations. When Van Rijn and Van den Berg applied their definitions to their own data, they obtained the interesting result that the reconstructed version and vergence contributions were effectively limited to two dimensions (2D). The version signal was confined to Listing's plane (no torsion) whereas the vergence signal remained within a horizontal-torsional plane (no vertical vergence). They showed theoretically that a model based on 2D version/2D vergence control will indeed produce the torsional eye positions in near fixations found in their experiments. This model cannot account for a second set of data in the literature [Mok, Ro, Cadera, Crawford & Vilis (1992) Vision Research, 32, 2055–2064]. With our definitions, we found that the simple 2D version/2D vergence control strategy cannot account for the Van Rijn and Van den Berg (1993) data but is nicely compatible with the considerably smaller amount of cyclotorsion in the data collected by Mok et al. (1992). We also show that, in such a system, having 2D vergence control is compatible with minimization of torsional disparity and provides the cyclovergence signals suitable for stabilizing the eyes in the non-Listing positions caused by a vertical saccade in near vision.

The oculomotor neural integrator uses a behavior-related coordinate system

Coordinate systems are a central issue in computational neuroscience: are they explicitly represented at some reductive level of brain function, and if so, are they only trivial products of associated anatomic geometries? This investigation examined these questions in the neural network that holds eye position, the so-called oculomotor integrator. Since neural activity in the integrator is behaviorally constrained by Listing's law to encode horizontal and vertical eye positions within Listing's plane and zero rotation about the orthogonal torsional axis, it was hypothesized that any integrator coordinate system would be developmentally predisposed to align with Listing's plane. A test for this hypothesis was developed with the use of a kinematically correct model of the three-dimensional saccade generator. Three mathematical integrators were used to represent the neuron populations that control torsional, vertical, and horizontal eye position. Simulated failure of the torsional and vertical integrators produced eye position drift that was parallel to the horizontal plane containing the intrinsic coordinate axes for these components. Furthermore, this drift settled toward a resting range parallel to the intrinsic vertical coordinate axis (for horizontal rotation). To experimentally identify these intrinsic population coordinates, three-dimensional eye positions were measured in four Macaca fascicularis after injection of muscimol into the mesencephalic interstitial nucleus of Cajal (INC), a technique that disrupts the torsional and vertical integrators (Crawford et al., 1991). INC inactivation produced exponential, position-dependent decay in vertical and torsional eye position. There was no position-dependent horizontal drift, but in the original coordinate system (defined arbitrarily by the measurement apparatus) there was a constant-direction horizontal drift. However, this extraneous horizontal drift was eliminated when the data were transformed into a coordinate system that aligned with Listing's plane. The direction of torsional drift correlated well (r = 0.85), across all experiments, with the normal to Listing's plane. On average, these two directions were only 0.06 degrees from perfect alignment. In contrast, drift direction did not correlate with stereotaxic coordinates (r = 0.10). Furthermore, the drift settled toward a range parallel to and correlated with Listing's plane (r = 0.94), whereas this range did not correlate well with stereotaxic coordinates (r = 0.02). On average, the resting range was aligned within 0.98 degrees of Listing's plane. Finally, this resting range was near orthogonal (average 91.9 degrees across all experiments) to the direction of torsional drift. These results show that integrator cell populations use an orthogonal, craniotopic coordinate system that aligns with Listing's plane.(ABSTRACT TRUNCATED AT 250 WORDS)

Changes of listing's plane and rapid eye movements after lesion of the rostral interstitial nucleus of the MLF

Changes of listing's plane and rapid eye movements after lesion of the rostral interstitial nucleus of the MLF

Three-dimensional analysis of strongly curved saccades elicited by double-step stimuli

Earlier recordings of eye position in three dimensions have revealed that Listing's law is obeyed in reasonable approximation, both statically and dynamically. This implies that all eye positions are confined to a plane when using a rotation vector or quaternion representation. The orientation of the angular velocity axis is crucial in order to preserve the law. For a single-axis rotation, the eye's angular velocity axis has to tilt out of Listing's plane, otherwise the law cannot be preserved in eccentric saccades. Experimental work has confirmed that normal, visually-guided saccades resemble single-axis rotations whose angular velocity axis tilts by the right amount. We investigated how well the saccadic system implements Listing's law when the trajectory of the eyes is more complicated, as in a non-single-axis rotation where the angular velocity vector depends on instantaneous eye position. Eye position was measured in three dimensions using the magnetic scleral search coil method for five subjects. Non-single-axis rotations of the eye were evoked with a double-step paradigm. We found that Listing's law is obeyed equally well during fixations, single-axis saccades and in non-single-axis saccades. Some deviations from the law were found in both curved and single-axis eye movements, but we demonstrated that the net torsional component of eye position of these saccades is negligible compared to that expected if the angular velocity axis did not tilt at all. In addition, analysis of the angular velocity signals in the curved movements showed strong similarity to the computed signal required for implementing Listing's law. Our results show that the observed deviations from Listing's law reflect only minor failures in the mechanism underlying its dynamic implementation. We conclude that single-axis rotations are not a necessary condition for the implementation of Listing's law in saccades. Our results are compatible with the notion that the implementation of Listing's law relies upon internal feedback. Various suggestions of how models can be reconciled with recent data on the three-dimensional control of saccades are discussed.

Rotation of Listing's plane during vergence

When visually fixating targets on an isovergence surface, the position of each eye was constrained to a plane. Thus, Listing's law holds during vergence. The planes were, however, rotated temporally with respect to those when viewing distant targets. The effect of this rotation was to produce a torsion which depended on eye elevation; extorsion of the two eyes for downward gaze and intorsion for upward gaze. The saccadic velocity command was relatively unaffected during vergence. Computer simulations suggest that the saccadic tonic command and the vergence command interact multiplicatively in three dimensions.

Symmetry of oculomotor burst neuron coordinates about Listing's plane.

1. The purpose of this investigation was to determine the axes of eye rotation generated by oculomotor burst neuron populations and the coordinate system that they collectively define. In particular, we asked if such coordinates might be related to constraints in the emergent behavior, i.e., Listing's law for saccades. 2. The mesencephalic rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) was identified in four monkeys with the use of single-unit recording, and then explored with the use of electrical microstimulation and pharmacological inactivation with the inhibitory gamma-aminobutyric acid (GABA) agonist muscimol. Three-dimensional (3-D) eye positions and velocities were recorded in one or both eyes while alert animals made eye movements in response to visual stimuli and head rotation. 3. Unilateral stimulation of the riMLF (20 microA, 200 Hz, 300-600 ms) produced conjugate, constant velocity eye rotations, which then stopped abruptly and held their final positions. This is expected if the riMLF produces phasic signals upstream from the oculomotor integrator. 4. Units that burst before upward or downward saccades were recorded intermingled in each side of the riMLF. Unilateral stimulation of the same riMLF sites produced eye rotations about primarily torsional axes, clockwise (CW) during right riMLF stimulation and counterclockwise (CCW) during left stimulation. Only small and inconsistent vertical components were observed, supporting the view that the riMLF carries intermingled up and down signals. 5. The torsional axes of eye rotation produced by riMLF stimulation did not correlate to external anatomic landmarks. Instead, stimulation axes from both riMLF sides aligned with the primary gaze direction orthogonal to Listing's plane of eye positions recorded during saccades. 6. Injection of muscimol into one side of the riMLF produced a conjugate deficit in saccades and quick phases, including a 50% reduction in all vertical velocities and complete loss of one torsional direction. CW was lost after right riMLF inactivation, and CCW was lost after left inactivation. 7. The plane that separated the intact torsional axes from the missing axes correlated with the orientation of Listing's plane. Thus, during left or right riMLF inactivation, the vertical axes of intact horizontal saccades were abnormally aligned with Listing's plane. The orientation of these axes was not correlated with external anatomic landmarks. 8. As suggested by their alignment with Listing's plane, the intact vertical axes of horizontal saccades following riMLF inactivation were orthogonal to torsional riMLF stimulation axes.(ABSTRACT TRUNCATED AT 400 WORDS)

Constraints on arm position when pointing in three dimensions: Donders' law and the Fick gimbal strategy.

1. While making saccades between targets with the head stationary, eye positions are constrained to two of the possible three degrees of freedom. Classically this constraint has been described by Donders' and Listing's laws. The objective was to determine whether these laws also apply for the straight arm when pointing between different targets. Thus we determined whether the arm adopts only one angular position for every pointing direction (Donders' law) and whether these positions can be described by rotations from a reference position about axes that lie in a plane (Listing's law). 2. The angular positions (orientations) of the arm in three-dimensional space were studied as subjects pointed with a straight arm at different targets. Arm position was measured with the search coil technique by means of coils attached to the back of the hand. Pointing was studied over a range of +/- 45 degrees in all directions from a central target located 45 degrees to the right of the straight-ahead position. 3. The positions of the arm in space were described by quaternion vectors, i.e., a particular position was described in terms of the axis and amplitude of a rotation from a reference position to that position. Using this description, it was found that the straight arm adopted a similar orientation (standard deviations ranged from 2.8 to 4.8 degrees) when pointing at a particular target irrespective of which target from which it had moved. 4. The angular position vectors for arm positions associated with relatively small movements (e.g., less than +/- 30 degrees) lay in a flat surface with minimal torsion. At first sight, this surface appeared to be similar to Listing's plane of the eye. However, for positions associated with larger movements (e.g., +/- 45 degrees) it became apparent that, unlike the eye, the surface deviated from one obeying Listing's law, i.e., it was twisted and showed torsion like that produced by rotations around the horizontal and vertical axes of a Fick gimbal. (The characteristic of a Fick gimbal is that the vertical axis is fixed, whereas the horizontal axis moves with the gimbal.) 5. Although there were differences between subjects, all showed a twisted position vector surface. The twist was always in the same direction, and it was always less than that of a Fick gimbal. 6. This position vector surface had a similar shape whether the arm was stationary or was moving between targets, whether subjects pointed with or without vision, and whether the pointing arm had moved between targets or from a bent-elbow position on the lap.(ABSTRACT TRUNCATED AT 400 WORDS)

Static roll and pitch in the monkey: Shift and rotation of listing's plane

In three rhesus monkeys three-dimensional eye positions were measured with the dual search coil technique. Recordings of spontaneous eye movements were made in the light and in the dark, with the monkeys in different static roll or pitch positions. Eye positions were expressed as rotation vectors. In all static positions eye rotation vectors were confined to a plane, i.e. Listing's plane was conserved. Tilt about the roll axis shifted the plane along this axis, i.e. a constant torsional component was added to all eye positions. Tilt about the pitch axis changed the pitch angle of Listing's plane.

Axes of eye rotation and Listing's law during rotations of the head

1. The vestibuloocular reflex (VOR) was examined in four alert monkeys during rotations of the head about torsional, vertical, horizontal, and intermediate axes. Eye positions and axes were recorded in three dimensions (3-D). Visual targets were used to optimize gaze stabilization. 2. Axes of eye rotation during slow phases showed small but systematic deviations from collinearity with the axes of head rotation. These noncollinearities apparently resulted from vector summation of torsional, vertical, and horizontal VOR components with different gains. 3. VOR gain was lowest about a head-fixed torsional axis that was correlated with the primary gaze direction, as determined by Listing's law for saccades. As a result, rotation of the head about a partially torsional axis produced noncollinear slow phases, with axes that tilted toward Listing's plane. 4. During slow phases, eye position changed not only in the direction of rotation, but also systematically in other directions. Even axes of eye rotation within Listing's plane caused eye position to move out of the plane to a torsional position that was then held. Thus Listing's law for saccades cannot be a product of plant mechanics. 5. VOR slow phases were simulated with the use of a model that incorporated 3-D rotational kinematics into the indirect path and the oculomotor plant. This demonstrated that the observed pattern of position changes is the expected consequence of rotating the eye about a fixed axis and that to hold these positions the indirect path must employ a 3-D velocity-to-position transformation. 6. Quick phases not only corrected the violations of Listing's law produced by slow phases but anticipated them by directing the eye toward a plane rotated in the direction of head rotation. This was modeled by inputting the vestibular signal to a Listing's law operator that is shared by the quick phase and saccadic systems.

Geometric relations of eye position and velocity vectors during saccades

Measurements of angular position and velocity vectors of the eye in three human and three monkey subjects showed that: (1) position vectors lie roughly in a single plane, in accordance with Listing's law, between and during saccades; (2) primary position of the eye is often far from the centre of the oculomotor range. (3) saccades have nearly-fixed rotation axes, which tilt out of Listing's plane in a systematic way depending on current eye position. Findings 1 and 3 show that saccadic control signals accurately reflect the properties of three-dimensional rotations, as predicted by a new quaternion model of the saccadic system; models that approximate rotational kinematics using vectorial addition and integration do not predict these findings.

Implications of rotational kinematics for the oculomotor system in three dimensions.

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)

Effect of gravitoinertial force on ocular counterrolling.

ArticleEffect of gravitoinertial force on ocular counterrolling.E F Miller 2nd, and A GraybielE F Miller 2nd, and A GraybielPublished Online:01 Nov 1971https://doi.org/10.1152/jappl.1971.31.5.697MoreSectionsPDF (995 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByOcular counter-roll is less affected in experienced versus novice space crew after long-duration spaceflight20 July 2022 | npj Microgravity, Vol. 8, No. 1The Role of Different Afferent Systems in the Modulation of the Otolith-Ocular Reflex After Long-Term Space Flights14 March 2022 | Frontiers in Physiology, Vol. 13Decreased otolith-mediated vestibular response in 25 astronauts induced by long-duration spaceflightEmma Hallgren, Ludmila Kornilova, Erik Fransen, Dmitrii Glukhikh, Steven T. Moore, Gilles Clément, Angelique Van Ombergen, Hamish MacDougall, Ivan Naumov, and Floris L. Wuyts10 June 2016 | Journal of Neurophysiology, Vol. 115, No. 6Human perceptual overestimation of whole body roll tilt in hypergravityTorin K. Clark, Michael C. Newman, Charles M. Oman, Daniel M. Merfeld, and Laurence R. Young3 April 2015 | Journal of Neurophysiology, Vol. 113, No. 7Dynamic characteristics of otolith ocular response during counter rotation about dual yaw axes in miceNeuroscience, Vol. 285Fusion of Visual and Vestibular Tilt Cues in the Perception of Visual VerticalR. A. A. Vingerhoets, M. De Vrijer, J. A. M. Van Gisbergen, and W. P. Medendorp1 March 2009 | Journal of Neurophysiology, Vol. 101, No. 3Space motion sickness5 October 2006 | Experimental Brain Research, Vol. 175, No. 3The subjective visual vertical and the perceptual upright21 March 2006 | Experimental Brain Research, Vol. 173, No. 4Is an Internal Model of Head Orientation Necessary for Oculomotor Control?9 January 2006 | Annals of the New York Academy of Sciences, Vol. 1039, No. 1Static and dynamic properties of vergence-induced reduction of ocular counter-roll in near visionEuropean Journal of Neuroscience, Vol. 21, No. 2Ocular torsion: rotations around the “WHY” axisJournal of American Association for Pediatric Ophthalmology and Strabismus, Vol. 8, No. 1Gravity Modulates Listing's Plane Orientation During Both Pursuit and SaccadesBernhard J.M. Hess, and Dora E. Angelaki1 August 2003 | Journal of Neurophysiology, Vol. 90, No. 2The Myth of Static Ocular Counter-RollingAnnals of the New York Academy of Sciences, Vol. 956, No. 1Plenary Lecture: Orientation of the Eyes to Gravitoinertial Acceleration25 January 2006 | Annals of the New York Academy of Sciences, Vol. 942, No. 1The Effect of Ocular Torsional Position on Perception of the Roll-tilt of Visual StimuliVision Research, Vol. 37, No. 8Determination of ocular torsion by means of automatic pattern recognitionIEEE Transactions on Biomedical Engineering, Vol. 43, No. 5Ocular torsion before and after 1 hour centrifugationBrain Research Bulletin, Vol. 40, No. 5-6Saccular impact on ocular torsionBrain Research Bulletin, Vol. 40, No. 5-6Linear Acceleration Modulates the Nystagmus Induced by Angular Acceleration Stimulation of the Horizontal CanalAnnals of the New York Academy of Sciences, Vol. 656, No. 1 Sensing and CVTM?a New Method of Measuring Ocular Torsion Using Image-Processing TechniquesAnnals of the New York Academy of Sciences, Vol. 656, No. 1 Sensing and CVTM — an image-processing system for measuring ocular torsionComputer Methods and Programs in Biomedicine, Vol. 35, No. 3Temporal Bone Pathology of a Patient without Hearing and Caloric Reaction, and with Counter-rolling after Chronic Myelocytic Leukemia8 July 2009 | Acta Oto-Laryngologica, Vol. 108, No. sup468PART II. THREE-DIMENSIONAL CODING IN THE OCULOMOTOR AND VISUAL SYSTEMS The Behavior of Human Gaze in Three Dimensions a17 December 2006 | Annals of the New York Academy of Sciences, Vol. 545, No. 1Ocular Torsional Movements in Normal HumansAmerican Journal of Ophthalmology, Vol. 95, No. 6Design Considerations for a Real-Time Ocular Counterroll InstrumentIEEE Transactions on Biomedical Engineering, Vol. BME-30, No. 5Ocular Torsion and the Primary Retinal MeridiansAmerican Journal of Ophthalmology, Vol. 91, No. 1Psychophysics of Vestibular SensationMeasurement of Otolith Function in Man More from this issue > Volume 31Issue 5November 1971Pages 697-700 https://doi.org/10.1152/jappl.1971.31.5.697PubMed5117183History Published online 1 November 1971 Published in print 1 November 1971 Metrics

SUPERIOR OBLIQUE MUSCLE-Reply

Dr. Jampel's letter was referred to Dr. Cohen who offers the following reply: To the Editor: Dr. Jampel objects to our conclusion that the functional insertion of the superior oblique muscle changes in adduction and abduction, and therefore that the axis of rotation of the globe shifts during superior muscle contraction in these positions. It is of interest that he came to a similar conclusion in 1963: axis of rotation of the individual extraocular muscles appear to vary with the position of the ( Invest Ophthal 2 :265-271, 1963). The functional insertion of the superior oblique is the point where the superior oblique tendon exerts force to move the globe. Due to the posterior lateral insertion of the tendon, it is behind the equatorial plane (Listing's plane) along the vertical optic axis plane in most positions of adduction or abduction. Given these relationships, the mechanics of the eye dictate