James S. Maxwell

Isovergence surfaces: the conjugacy of vertical eye movements in tertiary positions of gaze

Conjugate gaze is often defined as the equal angle rotation of the two eyes. For fixation at far distances, the optical axes are parallel and conjugacy is defined irrespective of the coordinate system. For nearby or finite fixation distances, the evaluation of conjugacy for many gaze postures depends on the coordinate system used to measure it. For example, if the eye is elevated or depressed and the eye is rotated about a vertical axis, the intersections of lines of sight with a tangent screen will describe either straight lines for arcs depending on whether the vertical axis is fixed with respect to the head or to the eye. Because of the horizontal separation of the two eyes, the binocular fixation of near targets at tertiary positions of gaze will require a vertical vergence component for head‐referenced but not eye‐referenced measurements. The vertical gaze alignment of three human subjects was measured as they viewed targets placed at secondary and tertiary eye positions at two different distances. Vertical vergence was either held open or closed‐loop. The lines of sight were found lo intersect (i.e. vertical gaze was aligned) regardless of target position or viewing condition.

Spatial aspects of vertical phoria adaptation

Vergence adaptation to vertical disparity spreads to unadapted directions of gaze. The spatial spread function for prism adaptation was estimated from aftereffects of a vertical disparity presented at a single position. Constraints limiting the spatial spread of adaptation were investigated with two stimuli of opposite disparity (hyper and hypo), presented at two different eye positions with a separation that varied from 6 to 18 deg in either the horizontal or vertical meridian. On average, phoria adaptation to the single point paradigm spread uniformly across the entire 18 deg test field. A resolution limit for adaptation to the two point paradigm was demonstrated by a reduction of phoria aftereffects with decreasing target separation (crowding). Vertical phoria aftereffects were reduced more by horizontal than by vertical crowding. A disparity gradient limit was demonstrated for a fixed target separation by a reduction of gain (phoria change/stimulus disparity) with increasing stimulus disparity.

Mechanisms of vertical phoria adaptation revealed by time-course and two-dimensional spatiotopic maps

The spatial spread of short term phoria adaptation was measured in response to either a single vertical disparity presented at a single eye position, or, vertical disparities of opposite sign presented at two different locations along either the primary vertical or horizontal meridians or along an oblique axis. The spread of adaptation to eye positions not specifically adapted was assessed by measuring phoria across a two-dimensional surface. The change in phoria was uniform across the field in response to a single disparity. With two disparities, adaptation conformed to the stimulus demand in the direction in which the disparity varied but was uniform in the orthogonal direction. The time-course of the adaptation indicated the presence of two mechanisms, a global one which shifted the phoria uniformly across the field and a local one which selectively adjusted the phoria to the position dependent demands of the disparity stimulus.

EYE POSITION SIGNALS IN THE ABDUCENS AND OCULOMOTOR NUCLEI OF MONKEYS DURING OCULAR CONVERGENCE

Many neurons in oculomotor pathways encode signals related to eye position. For example, motoneurons in the third, fourth, and sixth cranial nuclei discharge at highly regular rates during fixation intervals. During fixations of far targets, their tonic discharge is linearly related to conjugate eye position. Previous studies provided evidence that premotor cells in brainstem pathways also encoded conjugate eye position. McConville et al. (this volume), however, measured eye movements during binocular fixations when the eyes were converged and concluded that the position signal encoded by premotor position-vestibular-pause (PVP) cells in the vestibular nuclei is related to monocular (right or left) eye position rather than to conjugate eye position. This surprising relationship would not have been noticed in earlier studies that measured the movements of only one eye (using a single eye coil) or that measured only the conjugate movements of the two eyes (using bitemporal EOG electrodes). How general a feature of oculomotor signal processing is this finding? In this paper, we re-examine the eye position signal in abducens and oculomotor neurons when the movements of the two eyes are conjugate and when they are disjunctive and therefore disassociated. The data suggest that abducens neurons (AMNs and AINs) and oculomotor neurons (putative medial rectus motoneurons), unlike PVP cells, are not monocular but encode mixtures of right and left eye position signals.

Adaptation of vertical eye alignment in relation to head tilt

Binocular visual feedback is used to continually calibrate binocular eye alignment so that the retinal images of the two eyes remain in correspondence. Past experiments have shown that vertical eye alignment (measured as vertical phoria) can be altered by training to disparities that vary as a function of orbital eye position. The present experiments demonstrate that vertical eye alignment can also be trained to differ with head position when eye position (with respect to the orbit) is held constant. Changes in head position were about either an earth-vertical or earth-horizontal axis to distinguish otolith-ocular related adaptation from cervical-ocular related adaptation. Changes in head position were implemented by either by rotating the whole body (WB) or by rotating the head with the body stationary (HO). Following training, adaptation of eye alignment was observed in all cases of rotation about an earth-horizontal axis and for HO pitch rotations about an earth-vertical axis. The results illustrate the ability of the oculomotor system to compensate for imbalances in otolith-ocular pathways.

Plasticity of convergence-dependent variations of cyclovergence with vertical gaze

Binocular alignment of foveal images is facilitated by cross-couplings of vergence eye movements with distance and direction of gaze. These couplings reduce horizontal, vertical and cyclodisparities at the fovea without using feedback from retinal image disparity. Horizontal vergence is coupled with accommodation. Vertical vergence that aligns tertiary targets in asymmetric convergence is thought to be coupled with convergence and horizontal gaze. Cyclovergence aligns the horizontal retinal meridians during gaze elevation in symmetrical convergence and is coupled with convergence and vertical gaze. The latter vergence-dependent changes of cyclovergence have been described in terms of the orientation of Listings plane and have been referred to as the binocular extension of Listings law. Can these couplings be modified? Plasticity has been demonstrated previously for two of the three dimensions of vergence (horizontal and vertical). The current study demonstrates that convergence-dependent changes of the orientation of Listings plane can be adapted to either exaggerate or to reduce the cyclovergence that normally facilitates alignment of the horizontal meridians of the retinas with one another during gaze elevation in symmetrical convergence. The adaptability of cyclovergence demonstrates a neural mechanism that, in conjunction with the passive forces determined by biomechanical properties of the orbit, could play an active role in implementing Listings extended law and provide a means for calibrating binocular eye alignment in three dimensions.

A cross-coupling model of vertical vergence adaptation

Vertical disparity vergence aligns the two eyes in response to vertical misalignment (disparity) of the two ocular images. An adaptive response to vertical disparity vergence is demonstrated by the continuation of vertical vergence when one eye is occluded. The adaptive response is quantilied by vertical phoria, the eye alignment error during monocular viewing. Vertical phoria can be differentially adapted to vertical disparities of opposite sign located at two positions along the horizontal or vertical head-referenced axes. Vertical phoria aftereffects vary in amplitude as the eyes move from one adapted direction of gaze to another along the adaptation axis. A cross-coupling model was developed to account for the spatial variations of vertical phoria aftereffects. The model is constrained according to both single cell recordings of eye position sensitive neurons, and eye position measurements during and following adaptation. The vertieal phoria is computed by scaling the activities of eye position sensitive neurons and converting the scaled activities into a vertical vergence signal. The three components of the model are: neural activities associated with conjugate eye position, cross-coupling weights to scale the activities, and vertical vergence transducers to convert the weighted activities to vertical vergence. The model provides a biologically plausible mechanism for vertical vergence adaptation.

Changes in cyclotorsion and vertical eye alignment during prolonged monocular occlusion

When binocular vision is prevented with monocular occlusion, the two eyes assume a position of rest related to the combination of underlying tonic innervation of the oculomotor system, cross-coupled accommodative-vergence input and vergence responses to perceptual cues for spatial location relative to the head. When the latter two are controlled, the covered eye has been shown in the majority of subjects to turn outward (exophoria) and upward (hyperphoria) after prolonged monocular occlusion. The present study investigates the change in torsional eye alignment and its relation to vertical eye alignment after eight hours of monocular occlusion. The results revealed an excyclophoria during occlusion in four out of five subjects. The patched eye also became elevated in two subjects and depressed in two others. Thus, during prolonged monocular occlusion, the relative directions of cyclophoria and vertical phoria appear to be independent. In addition, there were non-concomitant changes in vertical phoria with horizontal gaze, toward a state where the adducted eye was elevated relative to the abducted eye. Simulations with Orbit(TM) suggest that these non-concomitant changes in vertical phoria with a concomitant excyclophoria may be based upon orbital mechanics. Excyclophoria appears to be the baseline state of binocular alignment.

Head-position-dependent Adaptation of Nonconcomitant Vertical Skew

Vertical phoria can be trained to vary with either head position or orbital eye position. The present experiments show that subjects can simultaneously adapt their eye-position-specific (nonconcomitant) vertical phorias in different directions at different head positions. Eye-position-dependent and head-position-dependent adaptive pathways, therefore, are not independent. Rather, the adaptation of vertical skew takes into account both eye and head position. In additional experiments, the magnitude of the nonconcomitant adaptive response was shown to be related to otolith output, increasing with head tilt ipsilateral to the tilt position at which training was received and decreasing in the contralateral direction.

The coordination of binocular eye movements: Vertical and torsional alignment

Precise binocular alignment of the visual axes is of utmost importance for good vision. The fact that so few of us ever experience diplopia is evidence of how well the oculomotor system performs this function in the face of changes due to development, disease and injury. The capacity of the oculomotor system to adapt to visual stimuli that mimic alignment deficits has been extensively explored in laboratory experiments. While the present paper reviews many of those studies, the primary focus is on issues involved in maintaining good vertical and torsional alignment in everyday viewing situations where the parsing of muscle forces may vary for the same horizontal and vertical eye positions due to changes in horizontal vergence and head posture.