Eye position compensation improves estimates of response magnitude and receptive field geometry in alert monkeys

Studies of visual function in behaving subjects require that stimuli be positioned reliably on the retina in the presence of eye movements. Fixational eye movements scatter stimuli about the retina, inflating estimates of receptive field dimensions, reducing estimates of peak responses, and blurring maps of receptive field subregions. Scleral search coils are frequently used to measure eye position, but their utility for correcting the effects of fixational eye movements on receptive field maps has been questioned. Using eye coils sutured to the sclera and preamplifiers configured to minimize cable artifacts, we reexamined this issue in two rhesus monkeys. During repeated fixation trials, the eye position signal was used to adjust the stimulus position, compensating for eye movements and correcting the stimulus position to place it at the desired location on the retina. Estimates of response magnitudes and receptive field characteristics in V1 and in LGN were obtained in both compensated and uncompensated conditions. Receptive fields were narrower, with steeper borders, and response amplitudes were higher when eye movement compensation was used. In sum, compensating for eye movements facilitated more precise definition of the receptive field. We also monitored horizontal vergence over long sequences of fixation trials and found the variability to be low, as expected for this precise behavior. Our results imply that eye coil signals can be highly accurate and useful for optimizing visual physiology when rigorous precautions are observed.     

An accurate and portable eye movement detector for studying sleep in small animals

Although eye movements are a highly valuable variable in attempts to precisely identify different periods of the sleep–wake cycle, their indirect measurement by electrooculography is not good enough. The present article describes an accurate and portable scleral search coil that allows the detection of tonic and phasic characteristics of eye movements in free‐moving animals. Six adult Wistar rats were prepared for chronic recording of electroencephalography, electromyography and eye movements using the scleral search coil technique. We developed a miniature magnetic field generator made with two coils, consisting of 35 turns and 15 mm diameter of insulated 0.2 mm cooper wire, mounted in a frame of carbon fibre. This portable scleral search coil was fixed on the head of the animal, with each magnetic coil parallel to the eye coil and at 5 mm from each eye. Eye movements detected by the portable scleral search coil were compared with those measured by a commercial scleral search coil requiring immobilizing the head of the animal. No qualitative differences were found between the two scleral search coil systems in their capabilities to detect eye movements. This innovative portable scleral search coil system is an essential tool to detect slow changes in eye position and miniature rapid eye movements during sleep. The portable scleral search coil is much more suitable for detecting eye movements than any previously available system because of its precision and simplicity, and because it does not require immobilization of the animal's head.     

Dynamic stabilization of receptive fields of cortical neurons (VI) during fixation of gaze in the macaque

Summary The positions of receptive field borders of striate cortical neurons were measured repeatedly in awake monkeys during attentive fixation of a small target. The border position, as marked by the onset of evoked activity in response to a moving stimulus, did not show the variability expected from previous measures of eye position variability during fixation. Measured variability was smaller than expected. Trial-by-trial comparisons suggest that receptive field borders are not shifted by the small eye movements occurring during attentive fixation. It is our hypothesis that attentive fixation engages a mechanism that gates incoming information to achieve a stabilization of the receptive field relative to the external world. Such a dynamic positional compensation may underlie preliminary evidence showing that the response of stereo-sensitive neurons in striate cortex is consistent with stimulus disparity measures and, within limits, does not reflect the retinal disparities produced by the changes in binocular alignment during fixation.     

Convergence eye movements evoked by microstimulation of the rostral superior colliculus in the cat

Results of our previous studies suggest that the circumscribed area in the rostral superior colliculus (SC) of the cat is involved in the control of accommodation. Accommodation is closely linked with vergence eye movements. In this study, we investigated whether or not vergence eye movements are evoked by microstimulation of the rostral SC in the cat. In addition, we studied the effect of chemical inhibition of the rostral SC on visually guided vergence eye movements. This study was conducted on three cats, weighing 2.5-3.5 kg. The animals were trained to carry out visually guided saccade and convergence tasks. Eye movements were measured using search coils placed on both eyes. We recorded eye movements evoked by microstimulation of the rostral SC in the alert cats. Muscimol was injected into the rostral SC, and the effect of SC inactivation on visually guided vergence eye movements was investigated. Convergence eye movements were evoked by low-current stimulation (< 30 microA) of a circumscribed area in the intermediate layers of the rostral SC on one side. Spontaneous saccades were interrupted by the stimulation of the low-threshold area for evoking convergence. Visually guided convergence eye movements were severely diminished by the injection of muscimol into the low-threshold area for evoking convergence of the SC. The rostral SC is related to the control of vergence eye movements as well as accommodation. The rostral SC may be involved in the functional linkage between accommodation, convergence and visual fixation.     

Antidromic identification of midbrain near response cells projecting to the oculomotor nucleus

Summary Medial rectus motoneurons carry both conjugate and vergence eye position signals. Abducens internuclear neurons, whose axons travel in the medial longitudinal fasciculus, provide these motoneurons with the major signal for conjugate eye movements but not for vergence eye movements. A vergence signal appropriate for these motoneurons is seen on the near response cells that are found in the mesencephalic reticular formation within 2 mm of the oculomotor nucleus. The goal of the present study was to determine if midbrain near response cells project to the medial rectus subdivision of the oculomotor nucleus. Near response cells were recorded in two trained rhesus monkeys with ocular search coils. A stimulating electrode was positioned within the medial rectus subdivision of the oculomotor nucleus. Twenty-eight near response cells were found that could be driven by single pulse microstimulation of the ipsilateral medial rectus subdivision. In all cases, antidromic activation was confirmed by collision testing. Attempts to antidromically activate midbrain near response cells from the contralateral medial rectus subdivision were unsuccessful. Most antidromically activated cells had a steady state firing rate proportional to vergence angle. One cell also showed burst activity during the vergence eye movements. Divergence cells were not antidromically activated.     

Small‐animal,whole‐body imaging with metamaterial‐inspired RF coil

Particular applications in preclinical magnetic resonance imaging require the entire body of an animal to be imaged with sufficient quality. This is usually performed by combining regions scanned with small coils with high sensitivity or long scans using large coils with low sensitivity. Here, a metamaterial‐inspired design employing a parallel array of wires operating on the principle of eigenmode hybridization was used to produce a small‐animal imaging coil. The coil field distribution responsible for the coil field of view and sensitivity was simulated in an electromagnetic simulation package and the coil geometrical parameters were optimized for whole‐body imaging. A prototype coil was then manufactured and assembled using brass telescopic tubes with copper plates as distributed capacitance. Its field distribution was measured experimentally using the B₁⁺ mapping technique and was found to be in close correspondence with the simulated results. The coil field distribution was found to be suitable for large field of view small‐animal imaging and the coil image quality was compared with a commercially available coil by whole‐body scanning of living mice. Signal‐to‐noise measurements in living mice showed higher values than those of a commercially available coil with large receptive fields, and rivalled the performance of small receptive field and high‐sensitivity coils. The coil was deemed to be suitable for some whole‐body, small‐animal preclinical applications.     

Visual responses of thalamic neurons depending on the direction of gaze and the position of targets in space

Summary Visual receptive field properties of neurons in the region of the thalamic internal medullary lamina were studied in alert cats while they fixated in various directions. In slightly more than 50% of the cells, the responsiveness of the cells was found to depend on the location of the stimulus with respect to the head-body axis (stimulus absolute position). A cell could ignore a stimulus outside its absolute field even if it was well placed within its receptive field.Three types of neurons were distinguished. Neurons with small central receptive fields were tonically activated when the animal fixated the stimulus in one half of the screen (usually contralateral). The firing rate of these cells was related to the stimulus absolute position measured along a preferred axis. Similarly, neurons with large receptive fields fired as a function of stimulus absolute position but stimulus fixation was not required. Neurons with eccentric fields responded to stimuli located in a target area defined in head-body coordinates. Such cells gave presaccadic bursts with eye movements terminating in the target area.The conclusion proposed is that neurons exist which code visual spatial information in a non-retinal frame of reference. This coding takes place at the time of stimulus presentation. Its role may be seen in the initiation of visually guided movements.     

Dynamics and efficacy of saccade-facilitated vergence eye movements in monkeys.

1. Four macaque monkeys were trained to fixate visual targets. Eye movements were recorded binocularly using the search coil technique. Saccades, vergence movements, and combinations of the two were elicited by training the monkeys to alternate the gaze between real visual targets that differed in viewing distance and eccentricity with respect to the monkeys' heads. 2. When they shifted the gaze between targets that were at different viewing distances, the monkeys made vergence eye movements. For targets placed along the midsagittal plane, the monkeys often made binocularly symmetric vergence movements. The peak speed of symmetric divergence movements increased linearly with vergence amplitude by 5.7 deg/s per degree of vergence. The peak speed of symmetric convergence movements increased linearly with vergence amplitude by 7.9 deg/s per degree of vergence. 3. For gaze shifts between targets placed eccentrically with respect to the midsagittal plane and at different viewing distances, the monkeys made saccades in combination with vergence eye movements. When a saccade occurred during a vergence movement, peak vergence eye speed increased abruptly and reached a peak that was proportional to the speed of the saccade. For four monkeys, peak divergence speed ranged from 242 to 315 deg/s and peak convergence speed ranged from 257 to 340 deg/s for 16-deg vergence and 20-deg saccadic eye movements. 4. For gaze shifts between far targets at the same viewing distance but different eccentricities, saccadic eye movements were transiently disjunctive even though there was no vergence requirement. Initially, the eyes diverged and then converged to restore fixation to the correct depth plane. Divergence was followed by convergence regardless of the direction of the saccade. 5. The presence of transient saccade-related disjunctive eye movements suggested that the abrupt increase in peak vergence speed during combined saccadic and vergence eye movements was produced by the linear addition of a vergence eye movement and the saccade-related transients. Consistent with this hypothesis, the rate of change in peak vergence speed during various-sized saccades between far targets (no vergence required) was similar to the rate of change in peak vergence speed during combined saccadic and vergence movements. However, the peak vergence speeds during the combined movements were higher than predicted by the linear addition hypothesis, suggesting the presence of an additional mechanism. 6. The saccade-related increase in peak vergence speed during combined saccades and vergences led to a significant decrease in the amount of time required to complete vergence movements.(ABSTRACT TRUNCATED AT 400 WORDS)     

Updating target distance across eye movements in depth

We tested between two coding mechanisms that the brain may use to retain distance information about a target for a reaching movement across vergence eye movements. If the brain was to encode a retinal disparity representation (retinal model), i.e., target depth relative to the plane of fixation, each vergence eye movement would require an active update of this representation to preserve depth constancy. Alternatively, if the brain was to store an egocentric distance representation of the target by integrating retinal disparity and vergence signals at the moment of target presentation, this representation should remain stable across subsequent vergence shifts (nonretinal model). We tested between these schemes by measuring errors of human reaching movements (n = 14 subjects) to remembered targets, briefly presented before a vergence eye movement. For comparison, we also tested their directional accuracy across version eye movements. With intervening vergence shifts, the memory-guided reaches showed an error pattern that was based on the new eye position and on the depth of the remembered target relative to that position. This suggests that target depth is recomputed after the gaze shift, supporting the retinal model. Our results also confirm earlier literature showing retinal updating of target direction. Furthermore, regression analyses revealed updating gains close to one for both target depth and direction, suggesting that the errors arise after the updating stage during the subsequent reference frame transformations that are involved in reaching.     

Scleral search coils influence saccade dynamics

The scleral search coil technique is commonly used for recording eye movements. The goal of this paper is to investigate to what extent the placement of scleral search coils onto the eyes influences the kinematics of saccades. To that end saccadic eye movements of human subjects were recorded with an infrared video system, while they wore coils and we compared the main sequence properties with recordings in which no coils were mounted on the eyes. It was found that saccades last longer (by about 8%) and become slower (by about 5%) when both eyes wear coils. This is truly due to the fact that the coils are on the eyes and not due to other factors that are part of this method, such as the scleral anesthesia. The influence of coils in both eyes was also observed when one coil was mounted on one eye only. Therefore the effect that the coils have on the eye movements cannot be attributed to purely mechanical factors, such as inertial load on the eyeball or increased friction. Rather the coils appear to change the oculomotor command signals that drive the saccadic eye movements.     

Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets

Neurons in the rostral superior colliculus (SC) of alert cats exhibit quasi-sustained discharge patterns related to the fixation of visual targets. Because some SC neurons also respond to auditory stimuli, we investigated whether there is a population of neurons in the rostral SC which is active in relation to fixation of both auditory and visual targets. We identified cells which were active with visual fixation and which continued to discharge if the fixation stimulus was briefly extinguished. The population of neurons exhibited similar discharge characteristics when the fixation stimulus was auditory. Few neurons were significantly more active during fixation of visual targets than during fixation of auditory targets. Most fixation neurons showed a diminished discharge rate during spontaneous (self-generated) saccadic eye movements away from a visual fixation stimulus, regardless of the direction of the saccade. this diminished discharge rate (or pause) typically began, on average, 12.2 ms before saccade onset and the duration of the pause was Ionger than the duration of the saccade. These observations are consistent with the hypothesis that increased discharge of these neurons is related to active fixation and that reductions in their activity are important for the generation of saccades. However, the lack of a precise relationship between pause duration and saccade duration implies that these neurons would be unlikely to project directly to the saccadic burst generator. The mean interval from the beginning of the pauses of fixation neurons to be beginning of the saccades away from fixation targets is also shorter than has been found in brainstem omnipause neurons. By analogy with the concept of a receptive field, agaze position error field depicts the range of gaze position error for which a cell is active. Although fixation neurons appear to encode the magnitude and direction of the error between visual targets and the visual axis, visual error fields at the end of fixating eye movements were significantly larger than those at stimulus onset. For auditory stimuli, this difference was not significant. These observations are compatible with a number of recent experiments indicating that neural signals of eye position are damped or delayed with respect to current eye position.     

Validity of Listing's law during fixations, saccades, smooth pursuit eye movements, and blinks

In its original formulation, Listing's law referred only to eye positions during steady fixation. In recent years, however, several studies have suggested that Listing's law can be extended to the movements of the eyes, including during saccades and smooth pursuit. A major problem in deciding whether or not Listing's law is obeyed during eye movements is the influence of any spontaneous fluctuations in torsional eye position. To try to settle this question, the three-dimensional position of the eyes (around the three axes: horizontal, vertical, and torsional) was recorded with dual search coils in five normal subjects during fixations, 20° saccades, blinks, and 20° pursuit movements with a 20°/s stimulus velocity. Eye movements across a wide range of horizontal positions were measured at different elevations of gaze during 11 min. Variability (as reflected in the standard deviation of torsional eye position) was used as a measure of the validity of Listing's law. After linear detrending single trials, each lasting 21.5 s, to remove the effects of drift over minutes, the reduction in the standard deviation of torsional position in tertiary eye positions was 54% assuming a planar and 58% assuming a second-order curved Listing's surface. We attributed this long-term fluctuation of the torsional signal to slippage of the coil on the eye. The remaining variability was mainly due to short-term fluctuation of eye torsion over seconds. The impact of hysteresis, associated with consecutive centrifugal-centripetal horizontal movements, on the variability of torsional eye position appeared negligible. Peak increases in the standard deviation from the fixation baseline after fitting individual Listing's planes for each trial were 348% during blinks, 141% during saccades, and 72% during pursuit movements (median value of five subjects). In conclusion, Listing's law during blinks, saccades, and pursuit is less valid than during fixations, which raises doubts about the existence of an internal Listing's law operator for eye movements. Possibly, central eye velocity commands do not comply with Listing's law.     

Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals

Based on the findings of the preceding paper, it is known that auditory and visual signals have been translated into common coordinates at the level of the superior colliculus (SC) and share a motor circuit involved in the generation of saccadic eye movements. It is not known, however, whether the translation of sensory signals into motor coordinates occurs prior to or within the SC. Nor is it known in what coordinates auditory signals observed in the SC are encoded. The present experiment tested two alternative hypotheses concerning the frame of reference of auditory signals found in the deeper layers of the SC. The hypothesis that auditory signals are encoded in head coordinates predicts that, with the head stationary, the response of auditory neurons will not be affected by variations in eye position but will be determined by the location of the sound source. The hypothesis that auditory responses encode the trajectory of the eye movement required to look to the target (motor error) predicts that the response of auditory cells will depend on both the position of the sound source and the position of the eyes in the orbit. Extracellular single-unit recordings were obtained from neurons in the SC while monkeys made delayed saccades to auditory or visual targets in a darkened room. The coordinates of auditory signals were studied by plotting auditory receptive fields while the animal fixated one of three targets placed 24 degrees apart along the horizontal plane. For 99 of 121 SC cells, the spatial location of the auditory receptive field was significantly altered by the position of the eyes in the orbit. In contrast, the responses of five sound-sensitive cells isolated in the inferior colliculus were not affected by variations in eye position. The possibility that systematic variations in the position of the pinnae associated with different fixation positions could account for these findings was controlled for by plotting auditory receptive fields while the pinnae were mechanically restrained. Under these conditions, the position of the eyes in the orbit still had a significant effect on the responsiveness of collicular neurons to auditory stimuli. The average magnitude of the shift of the auditory receptive field with changes in eye position (12.9 degrees) did not correspond to the magnitude of the shift in eye position (24 degrees). Alternative explanations for this finding were considered. One possibility is that, within the SC, there is a gradual transition from auditory signals in head coordinates to signals in motor error coordinates.(ABSTRACT TRUNCATED AT 400 WORDS)     

The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity

Summary The activity of 249 neurons in the dorsomedial frontal cortex was studied in two macaque monkeys. The animals were trained to release a bar when a visual stimulus changed color in order to receive reward. An acoustic cue signaled the start of a series of trials to the animal, which was then free to begin each trial at will. The monkeys tended to fixate the visual stimuli and to make saccades when the stimuli moved. The monkeys were neither rewarded for making proper eye movements nor punished for making extraneous ones. We found neurons whose discharge was related to various movements including those of the eye, neck, and arm. In this report, we describe the properties of neurons that showed activity related to visual fixation and saccadic eye movement. Fixation neurons discharged during active fixation with the eye in a given position in the orbit, but did not discharge when the eye occupied the same orbital positions during nonactive fixation. These neurons showed neither a classic nor a complex visual receptive field, nor a foveal receptive visual field. Electrical stimulation at the site of the fixation neurons often drove the eye to the orbital position associated with maximal activity of the cell. Several different kinds of neurons were found to discharge before saccades: 1) checking-saccade neurons, which discharged when the monkeys made self-generated saccades to extinguish LED's; 2) novelty-detection saccade neurons, which discharged before the first saccade made to a new visual target but whose activity waned with successive presentations of the same target. These results suggest that the dorsomedial frontal cortex is involved in attentive fixation. We hypothesize that the fixation neurons may be involved in codifying the saccade toward a target. We propose that their involvement in arm-eye-head motor-planning rests primarily in targeting the goal of the movement. The fact that saccaderelated neurons discharge when the saccades are self initiated, implies that this area of the cortex may share the control of voluntary saccades with the frontal eye fields and that the activation is involved in intentional motor processes.     

Analysis of retinal correspondence by studying receptive fields of rinocular single units in cat striate cortex

Summary The concept of corresponding retinal points was examined in terms of the binocular receptive fields of neurons in Area 17 of the cerebral cortex of the cat. Only a proportion of the binocular receptive field pairs can be accurately superimposed at the one time in a given plane. The fields which are not corresponding are said to show receptive field disparity. The attempt has been made to establish, on a quantitative basis, the parameters of the receptive field disparities that occur within 5° of the visual axis. A new method was used for defining the zero (vertical) meridian. Very effective paralysis of the extraocular muscles was achieved and the very small residual eye movements that occurred were regularly monitored so that corrections could be applied to the plotted positions of the receptive field pairs. The distribution of the receptive field disparities about the position of maximal correspondence has a range of about ±1.2° (S.D. 0.6°) in both the horizontal and vertical directions for fields in the vicinity of the visual axis. Panum's fusional area may represent the extent to which receptive fields in the one eye, all with the same visual direction, are linked to fellow members of a pair in the other eye over a range of receptive field disparities. A naso-temporal overlap of receptive fields occurs which is probably little if any more than can be accounted for on the basis of the disparity of receptive fields lying along the zero (vertical) meridian. When the extraocular muscles are paralyzed the eyes diverge and the binocular receptive field pairs are separated on the tangent screen. The distribution of the horizontal and vertical separations of the receptive field pairs have been examined.Selby Fellow of the Australian Academy of Sciences.     

The role of compensatory eye and head movements in the rat for image stabilization and gaze orientation

Compensatory horizontal eye movements of head restrained rats were compared with compensatory horizontal eye-head movements of partially restrained rats (head movements limited to the horizontal plane). Responses were evoked by constant velocity optokinetic and vestibular stimuli (10–60°/s) and recorded with search coils in a rotating magnetic field. Velocity and position components of eye and head responses were analysed. The velocity gains of optokinetic and vestibular responses of partially restrained and of head restrained rats were similarly high (between 0.8 and 1.0). Eye movements in partially restrained rats also contributed most (about 80%) to the velocity components of the responses. At stimulus velocities above 10°/s, the “beating field” of the evoked optokinetic and vestibular nystagmus was shifted transiently in the direction of ocular quick phases. The amplitude of this shift of the line of sight was about 3–10° in head restrained and about 20–30° in partially head restrained rats. Most of this large, transient gaze shift (about 80%) was accomplished by head movements. We interpret this gaze shift as an orienting response, and conclude that the recruitment of the ocular and the neck motor systems can be independent and task specific: head movements are primarily used to orient eye, ear and nose towards a sector of particular relevance, whereas eye movements provide the higher frequency dynamics for image stabilization and vergence movements.     

Vergence can be controlled by audio feedback,and induces downward ocular deviation

We measured horizontal and vertical eye positions, using binocular search coils, in three humans. Subjects could maintain vergence by means of audio biofeedback. Feedback consisted of a pair of audio tones, one variable and one fixed at a reference frequency. The variable tone was controlled by instantaneous vergence and provided immediate feedback on the vergence state. The reference frequency, which they attempted to match, was set to correspond to a target distance of either 0.34 m or 0.14 m. Subjects could maintain vergence consistently, even while undergoing lateral motions at 0.5 Hz and 0.2 g peak acceleration in darkness. There was also a consistent tendency for the eyes to deviate downward during near vergence. The results may be useful in experiments in which one wishes to control vergence without providing a visual reference which might inhibit conjugate eye movements.     

Resets of torsional eye position errors in different lighting conditions

To investigate a resetting mechanism of torsional eye position errors, spontaneous scanning eye movements and visually guided eye movements in different lighting conditions were recorded three dimensionally. Two monkeys (Macaca fuscata, TS, MI) were engaged in this experiment. A dual scleral search coil method was used for three-dimensional (3-D) eye movement recordings. In complete darkness, the thickness of Listing's plane at the onset of spontaneous saccades (0.51/0.37 degrees (TS/MI)) and that at the end of spontaneous fixation periods (0.47/0.34 degrees (TS/MI)) were significantly (P<0.001) smaller than that at the end of spontaneous saccades (0.59/0.45 degrees (TS/MI)) and that at the onset of spontaneous fixation periods (0.58/0.44 degrees (TS/MI)). Such differences in the thickness of Listing's plane were not observed in the light (P>0.10). Amplitude of torsional drift during post-saccadic fixation period was correlated with the amount of torsional position error at the end of saccade (P<0.001). The slope of regressed line in the dark or dim light (-0.40 to -0.50/-0.32 to -0.33 (TS/MI)) was steeper than that in the light (-0.04/-0.03 to -0.09 (TS/MI)). A resetting mechanism for torsional eye position errors during post-saccadic fixation periods is active in the dark but inactive in the light.     

Primate translational vestibuloocular reflexes. II. Version and vergence responses to fore-aft motion

To maintain binocular fixation on near targets during fore-aft translational disturbances, largely disjunctive eye movements are elicited the amplitude and direction of which should be tuned to the horizontal and vertical eccentricities of the target. The eye movements generated during this task have been investigated here as trained rhesus monkeys fixated isovergence targets at different horizontal and vertical eccentricities during 10 Hz fore-aft oscillations. The elicited eye movements complied with the geometric requirements for binocular fixation, although not ideally. First, the corresponding vergence angle for which the movement of each eye would be compensatory was consistently less than that dictated by the actual fixation parameters. Second, the eye position with zero sensitivity to translation was not straight ahead, as geometrically required, but rather exhibited a systematic dependence on viewing distance and vergence angle. Third, responses were asymmetric, with gains being larger for abducting and downward compared with adducting and upward gaze directions, respectively. As frequency was varied between 4 and 12 Hz, responses exhibited high-pass filter properties with significant differences between abduction and adduction responses. As a result of these differences, vergence sensitivity increased as a function of frequency with a steeper slope than that of version. Despite largely undercompensatory version responses, vergence sensitivity was closer to ideal. Moreover, the observed dependence of vergence sensitivity on vergence angle, which was varied between 2.5 and 10 MA, was largely linear rather than quadratic (as geometrically predicted). We conclude that the spatial tuning of eye velocity sensitivity as a function of gaze and viewing distance follows the general geometric dependencies required for the maintenance of foveal visual acuity. However, systematic deviations from ideal behavior exist that might reflect asymmetric processing of abduction/adduction responses perhaps because of different functional dependencies of version and vergence eye movement components during translation.     

Missing lateral rectus force and absence of medial rectus co-contraction in ocular convergence

For a given position of the eye in the orbit, most abducens motoneurons (LRMNs) fire at higher rates in converged gaze than when convergence is relaxed, implying that lateral rectus (LR) muscle force will be higher for a given eye position in convergence. If medial rectus (MR) muscle force balances LR force, it too would be higher in convergence, that is, LRMN recording studies predict horizontal rectus co-contraction in convergence. Three trained rhesus monkeys with binocular eye coils and custom muscle force transducers (MFTs) on LR and MR of one eye alternately fixated near (approximately 7 cm) and far (200 cm) targets with vergence movements of 20-30 degrees. Tonic muscle forces were also measured during conjugate fixation of far targets over a 30 x 30 degrees field. MFT characteristics and effects on oculomotility were assessed. Contrary to predictions, we found small (<1 g) decreases in both LR and MR forces in convergence, for those gaze positions that were used in the brain stem recording studies. This missing LR force paradox (higher LRMN firing rates in convergence but lower LR forces) suggests that motoneurons or muscle fibers contribute differently to oculorotary forces in converged and unconverged states, violating the final common path hypothesis. The absence of MR co-contraction is consistent with, and supports, the missing LR force finding. Resolution of the missing LR force paradox might involve nonlinear interactions among muscle fibers, mechanical specialization of muscle fibers and other articulations of the peripheral oculomotor apparatus, or extranuclear contributions to muscle innervation.