Combined Saccade-vergence Movements Research Articles

Response of supraoculomotor area neurons during combined saccade-vergence movements.

Combined saccade-vergence movements allow humans and other primates to align their eyes with objects of interest in three-dimensions. In the absence of saccades, vergence movements are typically slow, symmetrical movements of the two eyes in opposite directions. However, combined saccade-vergence movements produce vergence velocities that exceed values observed during vergence alone. This phenomenon is often called "vergence enhancement", or "saccade-facilitated vergence," though it is important to consider that rapid vergence changes, known as "vergence transients," are also observed during conjugate saccades. We developed a visual target array that allows monkeys to make saccades in all directions between targets spaced at distances that correspond to ~1° intervals of vergence angle relative to the monkey. We recorded the activity of vergence-sensitive neurons in the supra-oculomotor area (SOA), located dorsal and lateral to the oculomotor nucleus while monkeys made saccades with vergence amplitudes ranging from 0 to 10°. The primary focus of this study was to test the hypothesis that neurons in the SOA fire a high frequency burst of spikes during saccades that could generate the enhanced vergence. We found that individual neurons encode vergence velocity during both saccadic and non-saccadic vergence, yet firing rates were insufficient to produce the observed enhancement of vergence velocity. Our results are consistent with the hypothesis that slow vergence changes are encoded by the SOA while fast vergence movements require an additional contribution from the saccadic system. NEW & NOTEWORTHY Research into combined saccade-vergence movements has so far focused on exploring the saccadic neural circuitry, leading to diverging hypotheses regarding the role of the vergence system in this behavior. In this study, we report the first quantitative analysis of the discharge of individual neurons that encode vergence velocity in the monkey brain stem during combined saccade-vergence movements.

Saccadic amplitudes during combined saccade–vergence movements result from a weighted average of the target’s locations in the two retinas

Recent neurophysiological and behavioral studies have established that the saccadic amplitudes performed during combined saccade-vergence movements are unequal in the two eyes. These studies have not established, however, how the saccadic amplitude of each eye is determined. Our goal here is to fill this lacuna. We use three well-known metric attributes of saccadic movements as constraints and argue that the only quantitative model that obeys these constraints is one where each eye's saccadic amplitude is given by a weighted average of the target's locations in the two retinas. However, this theoretical result does not establish whether the weights in the weighted averaging operation are constant or whether they vary for different targets. To test the simpler of these two possibilities, namely the one of constant weights, we recorded combined saccade-vergence movements performed by human subjects. Our analysis of these movements shows that a constant-weights weighted averaging model provides an excellent description of their saccadic amplitudes. Overall, then, our conclusions are: (1) the two eyes' saccadic amplitudes are determined by weighted averages of the target's locations in the two retinas; (2) for targets within the oculomotor range of natural viewing, which was the range in our experiments, a weighted averaging model that uses constant weights accounts superbly for these saccadic amplitudes. We suggest that the weighted averaging operation that determines saccadic amplitudes is a by-product of a process whose purpose is to yoke the two eyes together. We provide a model explaining how this yoking may be achieved.

Evidence against the facilitation of the vergence command during saccade–vergence interactions

Combined saccade-vergence movements result when gaze shifts are made to targets that differ both in direction and in depth from the momentary fixation point. Currently, there are two rivaling schemes to explain these eye movements. According to the first, such eye movements are due to a combination of a conjugate saccadic command and a symmetric vergence command; the two commands are not taken to be independent but instead are suggested to interact in a nonlinear manner, which leads to an intra-saccadic facilitation of the vergence command. According to the second scheme, the saccade generator is disconjugate, thus encoding vergence information in the saccadic commands themselves, and the remaining vergence requirement is provided by an asymmetric mechanism. Here, we test the scheme that suggests an intra-saccadic facilitation of the vergence command. We analyze this scheme and show that it has two fundamental properties. The first is that the vergence command is always symmetric, even during the intra-saccadic facilitation. The second is that the facilitated (and symmetric) vergence command sums linearly with the conjugate saccadic command at the final common pathway. Taking these properties together, this scheme predicts that the total magnitude of the saccadic component of combined saccade-vergence movements can be decomposed into a conjugate part and a symmetric part. When we tested this prediction in combined saccade-vergence movements of humans, we found that it was not confirmed. Thus, our results are incompatible with the facilitation of the vergence command hypothesis. Although these results do not directly verify the rivaling hypothesis, which suggests a disconjugate saccade generator, they do provide it with indirect support.

Binocular coordination of saccades in children with vertigo: Dependency on the vergence state

The present study examines the quality of binocular coordination of saccades at far and near distance in 15 children with symptoms of vertigo headache and equilibrium disorders; these children show normal vestibular function but abnormal convergence eye movements (e.g., long time preparation, slow execution and poor accuracy, see Bucci, Kapoula, Yang, Bremond-Gignac, & Wiener-Vacher, 2004a, 2004b). The results show normal binocular saccade coordination at far distance, but large abnormal disconjugacy for saccades at near distance. During combined saccade–vergence movements (studied in six of these children), convergence remains abnormally slow. This supports the interpretation according to which poor binocular yoking of the saccades is linked to the reduced ability to produce fast convergence during the saccade; a learning mechanism based on rapid vergence would help to reduce the abducting–adducting asymmetry of the saccades. An alternative interpretation would be reduced learning ability for monocular adjustment of the saccade signals.

Latency of saccades, vergence, and combined movements in children with early onset convergent or divergent strabismus

The goal of this study was to examine latency of horizontal eye movements in the natural space (saccades, vergence, and combined saccade–vergence movements) in children with early onset convergent or divergent strabismus. Ten children were tested (8–11 years old): three with divergent strabismus, seven with convergent strabismus. A paradigm was used to elicit pure lateral saccades at far and near distance, pure vergence (convergence and divergence) and saccades combined with vergence movements. Horizontal eye movements from both eyes were recorded simultaneously by a photoelectric device (Oculometer, Dr. Bouis). The latency of saccades (at far and near distance), of vergence (convergence and divergence), and of combined movements greatly varies among subjects and has tendency to be longer than that observed in normal children of matched age, however, these differences reach significance in only a few cases. Children with divergent strabismus and residual gross binocular vision show abnormally longer vergence latencies than children with convergent strabismus without binocular vision. The initiation of combined movements does not show a dominant pattern, such as preceding vergence, as is found in normal children. Finally, strabismus surgery has no major effect on latencies. We conclude that there is no overall deficiency in latencies of eye movements in 3D space in children with early onset strabismus. Most likely, monocular visual input can be efficient as normal binocular vision for vergence movements. In a few subjects with divergent strabismus and fragile, intermittent binocular vision, latencies can be abnormally long, just because of the fragile binocular input and/or attention effort needs to use it. The absence of a pattern of initiation similar to normal children could be due to attention and fixation capabilities.

Directional Asymmetry During Combined Saccade–Vergence Movements

We investigated relationships between saccadic and vergence components of gaze shifts as 10 human subjects switched visual fixation between targets aligned in the midsagittal plane that lay in different vertical directions and at different distances. When fixation was shifted between a higher distant target and a lower near target, peak convergence velocity followed peak vertical saccadic velocity by a median interval of 12 ms. However, when fixation was shifted between a lower distant target and a higher near target, peak convergence velocity followed peak vertical saccadic velocity by a median interval of 76 ms. For the 2 stimulus arrangements, the median intervals by which peak divergence velocity followed the peak vertical saccadic velocity were 4 and 20 ms, respectively. The dissociation interval between the peak velocities of convergence and upward saccades increased with vertical saccade size, required convergence angle, and elevation of the endpoint of the movement. Velocity waveforms of vergence responses were more skewed when peak velocity was closely associated with saccadic peak velocity than when the vergence responses were delayed. Convergence peak velocities did not vary in any consistent pattern, but divergence peak velocities were generally smaller with responses that were delayed. Vergence movements were accompanied by small, high-frequency conjugate oscillations, suggesting that omnipause neurons were inhibited for both types of responses. In conclusion, the present findings indicate that the dynamic properties of horizontal vergence movements depend on the direction and timing of vertical saccades; these findings suggest experimental tests for current models of saccade-vergence interaction.

Ocular oscillations generated by coupling of brainstem excitatory and inhibitory saccadic burst neurons.

The human saccadic system is potentially unstable and may oscillate if the burst neurons, which generate saccades, are not inhibited by omnipause neurons. A previous study showed that combined saccade vergence movements can evoke oscillations in normal subjects. We set out to determine: 1) whether similar oscillations can be recorded during other paradigms associated with inhibition of omnipause neurons; 2) whether lesions of the fastigial nuclei disrupt such oscillations; and 3) whether such oscillations can be reproduced using a model based on the coupling of excitatory and inhibitory burst neurons. We recorded saccadic oscillations during vergence movements, combined saccade-vergence movements, vertical saccades, pure vergence and blinks in three normal subjects, and in a patient with saccadic hypermetria due to a surgical lesion affecting both fastigial nuclei. During combined saccade-vergence, normal subjects and the cerebellar patient developed small-amplitude (0.1 - 0.5 degrees), high-frequency (27-35 Hz), conjugate horizontal saccadic oscillations. Oscillations of a similar amplitude and frequency occurred during blinks, pure vergence and vertical saccades. One normal subject could generate saccadic oscillations voluntarily (approximately 0.7 degrees amplitude, 25 Hz) during sustained convergence. Previous models proposed that high-frequency eye oscillations produced by the saccadic system (saccadic oscillations), occur because of a delay in a negative feedback loop around high-gain, excitatory burst neurons in the brainstem. The feedback included the cerebellar fastigial nuclei. We propose another model that accounts for saccadic oscillations based on 1) coupling of excitatory and inhibitory burst neurons in the brainstem and 2) the hypothesis that burst neurons show post-inhibitory rebound discharge. When omnipause neurons are inhibited (as during saccades, saccade-vergence movements and blinks), this new model simulates oscillations with amplitudes and frequencies comparable to those in normal human subjects. The finding of saccadic oscillations in the cerebellar patient is compatible with the new model but not with the recent models including the fastigial nuclei in the classic negative-feedback loop model. Our model proposes a novel mechanism for generating oscillations in the oculomotor system and perhaps in other motor systems too.

Latency of saccades, vergence and combined saccade vergence movements in a subject with manifest latent nystagmus

purpose To study eye movements in 3D space – saccades, vergence and combined eye movements – in a subject with Manifest Latent Nystagmus (MLN).methods A 13-year-old girl diagnosed with MLN participated in this study. Saccades, pure vergence along the median plane and combined saccade-vergence movements were recorded under both binocular and monocular viewing. Horizontal eye movements from both eyes were recorded simultaneously with a photoelectric device (Bouis Oculometer).results The recordings of saccades, vergence or both components of combined movements show that such movements have a staircase trajectory. The consequence of this staircase behavior is that the time for approaching the target is prolonged. The latency of all types of eye movements is extended when the subject is viewing binocularly, while latency values are normal when viewing monocularly; the difference between the viewing conditions is significant for vergence.conclusion The normal latency values under monocular viewing are attributed to facilitation of eye movement initiation by the increased nystagmus.

Gap effects on saccade and vergence latency.

To explore visual space, we make saccades, vergence, and, most frequently, combined saccade-vergence eye movements. The initiation of saccades is well studied, while that of vergence is less explored. Saccade latency is influenced by the fixation task: when the target appears simultaneously with the offset of the fixation point, latencies tend to be regular, whereas the introduction of a gap period before target onset causes the emergence of express latencies (80- to 120-ms). This study examines in ten normal adults whether the gap paradigm has a similar effect on the latency of vergence and combined eye movements. The second goal is to identify contextual factors that favor the emergence of short latencies, by comparing a condition in which gap and simultaneous trials were performed in separate blocks (pure blocks) with a condition in which the two types of trials were interleaved randomly (mixed blocks). The results are: (1) the gap paradigm reduced similarly (by approximately -30 ms) the mean latency of saccades, convergence, divergence, and both the saccadic and vergence components of combined eye movements; (2) the gap paradigm was responsible for the emergence of 80- to 120-ms latencies for saccades and divergence (pure or combined), but rarely for convergence; (3) inspection of the latency distributions showed that such short latencies formed a clearly distinct population, different from anticipatory responses or regular latencies, for saccades (pure or combined) but not for pure vergence; importantly, distinct express latencies were found also for the convergence and divergence components of combined eye movements; (4) no difference was found for the group of subjects between pure and mixed blocks, but the latter yielded shorter latencies for some subjects, suggesting an idiosyncratic phenomenon. We suggest that distinct express latencies are specific to saccades and could correspond to a specific mode of saccade initiation. Interestingly, the express mode of triggering can be transferred to the vergence component in the ecological condition in which saccade is combined with vergence.

Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus.

Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus. This study investigated the role of the monkey superior colliculus (SC) in the control of visually (V)-guided combined saccade-vergence movements by assessing the perturbing effects of microstimulation. We elicited an electrical saccade (E) by stimulation (in 20% of trials) in the SC while the monkey was preparing a V-guided movement to a near target. The target was aligned such that E- and V-induced saccades had similar amplitudes but different directions and such that V-induced saccades had a significant vergence component (saccades to a near target). The onset of the E-stimulus was varied from immediately after V-target onset to after V-saccade onset. E-control trials, where stimulation was applied during fixation of a V-target, yielded the expected saccade but no vergence. By contrast, early perturbation trials, where the E-stimulus was applied soon after the onset of the V-target, caused an E-triggered response with a clear vergence component toward the V-target. Midflight perturbation, timed to occur just after the monkey initiated the movement toward the target, markedly curtailed the ongoing vergence component during the saccade. Examination of pooled responses from both types of perturbation trials showed weighted-averaging effects between E- and V-stimuli in both saccade and fast vergence components. Both components exhibited a progression from E- to V-dominance as the E-stimulus was delayed further. This study shows that artificial intervention in the SC, while a three-dimensional (3D) refixation is being prepared or is ongoing, can affect the timing (WHEN) and the metric specification (WHERE) of both saccades and vergence. To explain this we interpret the absence of overt vergence in the E-controls as being caused by a zero-vergence change command rather than reflecting the mere absence of a collicular vergence signal. In the perturbation trials, the E-evoked zero-vergence signal competes with the V-initiated saccade-vergence signal, thereby giving rise to a compromised 3D response. This effect would be expected if the population of movement cells at each SC site is tuned in 3D, combining the well-known topographical code for direction and amplitude with a nontopographical depth representation. On E-stimulation, the local population would yield a net saccade signal caused by the topography, but the cells coding for different depths would be excited equally, causing the vergence change to be zero.

Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position.

1. Monkeys were trained to look to brief visual targets presented in a completely darkened room. On some trials, after the visual target disappeared but before a saccade to the target could be initiated, the eyes were driven to another position in the orbit by electrical stimulation of the superior colliculus. Retinocentric models of the saccadic system predict that a saccade with a predetermined distance and direction based entirely on retinal error will occur. If this were the case, gaze would miss the target location by a distance and direction equal to the vector of the stimulation-induced movement. Spatial models assume that the retinal error signal will be combined with information about the change in eye position produced by stimulation and predict that the animal will look to the position of the target in space. 2. Results confirm the predictions of spatial models. Animals compensated for the stimulation-induced perturbation by looking to the position of the target in space. The result predicted by retinocentric models-a saccade with a direction and amplitude based on retinal error alone-was never observed. 3. The eye movement that compensated for the change in eye position produced by stimulation was a saccade, not a passive, lowvelocity movement to an orbital position of mechanical equilibrium established by a tonic pattern of motoneuron activation specified by the visual target. This indicates that a new saccade command, based on stored information about the location of the retinal image and information about the new position of the eyes, had been issued. Computation of the vector of the compensatory saccade does not necessarily increase the latency of target acquisition. The interval between the end of a stimulation-induced saccade and the beginning of the compensatory saccade was frequently 20 ms or less, permitting the animal to acquire the target with a normal latency.

Colliculoreticular organization in primate oculomotor system

Colliculoreticular organization in primate oculomotor system

Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey.

RECENT SINGLE-UNIT recording studies of the alert rhesus monkey superior colliculus have disclosed that the deeper layers of this structure contain cells which discharge in association with eye movement (15-17, 23, 24). Such units fire selectively prior to saccades of a specific direction and size, irrespective of the position of the eye in orbit. Stimulation studies of the superior colliculus have so far produced conflicting results. Some reports suggest that in the alert cat stimulation brings the eye to a certain position in orbit irrespective of eye position prior to stimulation (1, 9, 19). Thus, the size and direction of elicited saccades is reported to vary as a function of initial eye position. By contrast, in the alert monkey it has recently been reported that stimulation produces conjugate saccades of a specific size and direction; these parameters are the same no matter where the eye is in the orbit prior to stimulation (12, 15, 16). The stimulation map of Robinson (12) shows a reasonable correspondence with the receptive-field map of the superior colliculus reported by Cynader and Berman (5). The aim of this study was to clarify the relationship between recording and stimulation data by using methods which allow a direct comparison. We used alert rhesus monkeys which had one eye immobilized for the mapping of visual receptive fields. The other eye was normal, thus permitting the study of eye movement. Stimulation and recording were carried out using the same low-resistance microelectrode; for each site sampled, records were obtained for both single-unit activity and for electrical stimulation.