Pontine Omnipause Activity During Conjugate and Disconjugate Eye Movements in Macaques

2003 ◽  
Vol 90 (6) ◽  
pp. 3838-3853 ◽  
Author(s):  
C. Busettini ◽  
L. E. Mays

Previous reports have shown that saccades executed during vergence eye movements are often slower and longer than conjugate saccades. Lesions in the nucleus raphe interpositus, where pontine omnipause neurons (OPNs) are located, were also shown to result in slower and longer saccades. If vergence transiently suppresses the activity of the OPNs just before a saccade, then reduced presaccadic activity might mimic the behavioral effects of a lesion. To test this hypothesis, 64 OPNs were recorded from 7 alert rhesus monkeys during smooth vergence and saccades with and without vergence. The firing rate of many OPNs was modulated by static vergence angle but not by version and showed transient changes during slow vergence without saccades. This modulation was smooth, and not the abrupt pause seen for saccades, indicating that OPNs do not act as gates for vergence commands. We confirmed that saccades made during both convergence and divergence are significantly slower and longer than conjugate saccades. OPNs paused for all saccades, and the pause lead (interval between pause onset and saccadic onset) was significantly longer for saccades with convergence, in agreement with our hypothesis. Contrary to our hypothesis, pause lead was not longer for saccades with divergence, even though these saccades were slowed as much as those occurring during convergence. Furthermore, there was no significant correlation, on a trial-by-trial basis, between pause lead and saccadic slowing. These results suggest that it is unlikely that presaccadic slowing of OPNs is responsible for the slower saccades seen during vergence movements.

1984 ◽  
Vol 51 (5) ◽  
pp. 1091-1108 ◽  
Author(s):  
L. E. Mays

Animals with binocular single vision use disjunctive (vergence) eye movements to align the two eyes on a visual target. Several lines of evidence suggest that conjugate and vergence eye movement commands are generated independently and combined at the medial rectus motoneurons. If this were true, then a pure vergence eye-position signal should exist. This signal would be proportional to the horizontal angle between the eyes (vergence angle), without regard to the direction of conjugate gaze. The purpose of this experiment was to identify and study neurons that carry a pure vergence signal. Extracellular unit recordings were made from midbrain and pontine sites in monkeys trained to track visual targets moving in the horizontal, vertical, and depth (or target vergence) planes. The most commonly encountered neuron that had a vergence signal was the convergence cell. These units had a firing rate that was linearly proportional to the convergence angle; their activity was unaffected by changes in conjugate gaze. Changes in convergence cell activity preceded the change in vergence angle slightly. Convergence cell activity increased for increased convergence regardless of whether the change was in response to purely accommodative or disparity cues. Divergence cells were found far less frequently. These cells were similar to convergence cells except that they decreased their firing rate for increases in convergence. The activity of divergence cells was unaffected by changes in the direction of conjugate gaze. Both convergence and divergence cells were found, intermixed, in the mesencephalic reticular formation must outside the oculomotor nucleus. Most cells with a vergence signal were found within 1-2 mm of the nucleus. These results support the view that conjugate and vergence signals are generated independently and are combined at the extraocular motoneurons. Convergence cells seem ideally suited to provide the vergence signal required by the nearby medial rectus motoneurons.


2005 ◽  
Vol 94 (4) ◽  
pp. 2295-2311 ◽  
Author(s):  
C. Busettini ◽  
L. E. Mays

Horizontal vergence eye movements are movements in opposite directions used to change fixation between far and near targets. The occurrence of a saccade during vergence causes vergence velocity to be transiently enhanced. The goal of this study was to test in the monkey the previously described Multiply Model (Zee et al. 1992) that holds that, in humans, the speeding of vergence during a saccade may be the result of the disinhibition of a subgroup of vergence-related neurons by the saccadic omnipause neurons (OPNs). In agreement with the Multiply Model: 1) the onset of the enhancement was closely related to saccadic onset, and thus linked to the onset of the OPN pause; 2) the magnitude of the vergence velocity enhancement was strongly dependent on saccade–vergence timing. Contrary to the Multiply Model: 1) the peak of the vergence velocity enhancement was dependent on saccadic peak velocity; 2) the dependency on saccadic peak velocity was not the indirect result of a dependency on saccadic duration and therefore on the duration of the OPN pause; 3) the decline of the vergence enhancement, identified by the time of the peak of the enhancement velocity, occurred too early to be linked to the end of the OPN pause; 4) vergence enhancement had a saccadic-like peak-velocity/size main sequence. Overall, the evidence is incompatible with the OPN Multiply hypothesis of vergence enhancement. Alternative models are described in an accompanying paper.


1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen

The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement–based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + rE˙, where FR is firing rate, E and E˙ are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or “slide” (FR = b + kE + rE˙ + uË − c[Formula: see text]), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients ( r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias ( b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.


1976 ◽  
Vol 39 (6) ◽  
pp. 1246-1256 ◽  
Author(s):  
L. Ritchie

1. Areas of cerebellar cortex related to saccadic eye movements were ablated in three Macaca mulatta monkeys trained to fixate visual targets. There followed a postoperative dysmetria of saccadic eye movements which appeared to be the result of an impairment specifically within the saccadic system. 2. Convergent evidence from two experimental paradigms indicated that the saccadic deficit was a function of the position of the eye in the orbit and did not involve retinal error processing. 3. The pattern of this position-dependent dysmetria suggests that the eye was no longer fully compensating for the elastic restoring forces imposed by the orbital medium and antagonist muscle(s). 4. The similarity of these data to saccadic eye movements of human cerebellar patients and arm movements of rhesus monkeys with cerebellar lesions indicates that the inability to compensate for the differential loads placed on motor systems by the mechanics of those systems may explain several cerebellar symptoms.


2002 ◽  
Vol 88 (4) ◽  
pp. 1880-1892 ◽  
Author(s):  
M. Missal ◽  
E. L. Keller

The premotor pathways subserving saccades and smooth-pursuit eye movements are usually thought to be different. Indeed, saccade and smooth-pursuit eye movements have different dynamics and functions. In particular, a group of midline cells in the pons called omnipause neurons (OPNs) are considered to be part of the saccadic system only. It has been established that OPNs keep premotor neurons for saccades under constant inhibition during fixation periods. Saccades occur only when the activity of OPNs has completely stopped or paused. Accordingly, electrical stimulation in the region of OPNs inhibits premotor neurons and interrupts saccades. The premotor relay for smooth pursuit is thought to be organized differently and omnipause neurons are not supposed to be involved in smooth-pursuit eye movements. To investigate this supposition, OPNs were recorded during saccades and during smooth pursuit in the monkey ( Macaca mulatta). Unexpectedly, we found that neuronal activity of OPNs decreased during smooth pursuit. The resulting activity reduction reached statistical significance in ∼50% of OPNs recorded during pursuit of a target moving at 40°/s. On average, activity was reduced by 34% but never completely stopped or paused. The onset of activity reduction coincided with the onset of smooth pursuit. The duration of activity reduction was correlated with pursuit duration and its intensity was correlated with eye velocity. Activity reduction was observed even in the absence of catch-up saccades that frequently occur during pursuit. Electrical microstimulation in the OPNs' area induced a strong deceleration of the eye during smooth pursuit. These results suggest that OPNs form an inhibitory mechanism that could control the time course of smooth pursuit. This inhibitory mechanism is part of the fixation system and is probably needed to avoid reflexive eye movements toward targets that are not purposefully selected. This study shows that saccades and smooth pursuit, although they are different kinds of eye movements, are controlled by the same inhibitory system.


1991 ◽  
Vol 66 (6) ◽  
pp. 2125-2140 ◽  
Author(s):  
A. M. Pastor ◽  
B. Torres ◽  
J. M. Delgado-Garcia ◽  
R. Baker

1. The discharge of antidromically identified medial rectus and abducens motoneurons was recorded in restrained unanesthesized goldfish during spontaneous eye movements and in response to vestibular and optokinetic stimulation. 2. All medial rectus and abducens motoneurons exhibited a similar discharge pattern. A burst of spikes accompanied spontaneous saccades and fast phases during vestibular and optokinetic nystagmus in the ON-direction. Firing rate decreased for the same eye movements in the OFF-direction. All units showed a steady firing rate proportional to eye position beyond their recruitment threshold. 3. Motoneuronal position (ks) and velocity (rs) sensitivity for spontaneous eye movements were calculated from the slope of the rate-position and rate-velocity linear regression lines, respectively. The averaged ks and rs values of medial rectus motoneurons were higher than those of abducens motoneurons. The differences in motoneuronal sensitivity coupled with structural variations in the lateral versus the medial rectus muscle suggest that symmetric nasal and temporal eye movements are preserved by different motor unit composition. Although the abducens nucleus consists of distinct rostral and caudal subgroups, mean ks and rs values were not significantly different between the two populations. 4. Every abducens and medial rectus motoneuron fired an intense burst of spikes during its corresponding temporal or nasal activation phase of the "eye blink." This eye movement consisted of a sequential, rather than a synergic, contraction of both vertical and horizontal extraocular muscles. The eye blink could act neither as a protective reflex nor as a goal-directed eye movement because it could not be evoked in response to sensory stimuli. We propose a role for the blink in recentering eye position. 5. Motoneuronal firing rate after ON-directed saccades decreased exponentially before reaching the sustained discharge proportional to the new eye position. Time constants of the exponential decay ranged from 50 to 300 ms. Longer time constants after the saccade were associated with backward drifts of eye position and shorter time constants with onward drifts. These postsaccadic slide signals are suggested to encode the transition of eye position to the new steady level. 6. Motoneurons modulated sinusoidally in response to sinusoidal head rotation in the dark, but for a part of the cycle they went into cutoff, dependent on their eye position recruitment threshold. Eye position (kv) and velocity (rv) sensitivity during vestibular stimulation were measured at frequencies between 1/16 and 2 Hz. Motoneuronal time constants (tau v = rv/kv) decreased on the average by 25% with the frequency of vestibular stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)


1982 ◽  
Vol 47 (5) ◽  
pp. 827-844 ◽  
Author(s):  
C. Evinger ◽  
C. R. Kaneko ◽  
A. F. Fuchs

1. In the cats trained to follow a target spot with their eyes, activity was recorded from omnipause neurons (OPNs). OPNs discharge at a relatively high steady tonic rate (50-130 spikes/s) during visual fixation and smooth-pursuit eye movements but exhibit a complete cessation of discharge that begins before saccades in any direction. They are located in a compact region of the dorsal pontine tegmentum near the midline, just rostral to the abducens nucleus. 2. The average duration of the horizontal or vertical component of a saccade increases monotonically with pause duration, but a given pause duration is associated with a large range of individual saccade parameters and the timing of the pause, such as the latency from the pause onset to saccade onset or the interval from the maximum saccade velocity to the end of the pause, is no better. However, OPNs can be divided into two distinct groups on the basis of the timing of the pause relative to the parameters of the saccade. One group ceases discharging 32.4 +/- 4.6 ms, on average, before the saccade, while the second pauses 18.2 +/- 3.4 ms before the saccade. 3. Microstimulation at the site of OPNs affects the occurrence and trajectory of saccades but not smooth pursuit or fixation. Sustained electrical stimulation (20 micro A) lasting several seconds prevents the occurrence of saccades while brief trains (10-60 ms), timed to occur early in the saccade, interrupt it in midflight for the duration of the train. The latency to the interruption is about 26 ms. These data support the view that OPNs tonically inhibit the saccadic machinery between saccades and must be turned off to allow a saccade to occur. 4. Almost every (65 of 69) feline OPN exhibited a brief transient increase in activity for visual stimuli moving in any direction with a wide range of velocities. A moving 1 degree spot was generally more effective than a moving full-field, striped background. All units also showed a transient increase in firing when the spot was turned either on or off. Receptive fields plotted with the spot were greater than 250 deg2 and always included the area centralis. Two-thirds of the cells tested also responded to auditory stimuli. 5. Interaction between the excitatory visual input and the saccade-related pause was tested by comparing OPN activity and the saccadic trajectory during eye movements in the dark versus the light and by presenting brief flashes of light during a saccade. During saccades in the dark, the steady firing of OPNs was less than during saccades in the light. Only by stabilizing a flashed spot of light to occur on the area centralis at the beginning of the saccade was it possible to activate an OPN artificially to interrupt the saccade in midflight. Therefore, rather than being instrumental in specifically controlling the saccade trajectory, the visual input, along with the auditory and other sensory inputs, probably serves, under normal visual conditions, to help establish the tonic rate of OPNs. 6...


2010 ◽  
Vol 103 (3) ◽  
pp. 1171-1178 ◽  
Author(s):  
Nicholas A. Steinmetz ◽  
Tirin Moore

The visually driven responses of macaque area V4 neurons are modulated during the preparation of saccadic eye movements, but the relationship between presaccadic modulation in area V4 and saccade preparation is poorly understood. Recent neurophysiological studies suggest that the variability across trials of spiking responses provides a more reliable signature of motor preparation than mean firing rate across trials. We compared the dynamics of the response rate and the variability in the rate across trials for area V4 neurons during the preparation of visually guided saccades. As in previous reports, we found that the mean firing rate of V4 neurons was enhanced when saccades were prepared to stimuli within a neuron's receptive field (RF) in comparison with saccades to a non-RF location. Further, we found robust decreases in response variability prior to saccades and found that these decreases predicted saccadic reaction times for saccades both to RF and non-RF stimuli. Importantly, response variability predicted reaction time whether or not there were any accompanying changes in mean firing rate. In addition to predicting saccade direction, the mean firing rate could also predict reaction time, but only for saccades directed to the RF stimuli. These results demonstrate that response variability of area V4 neurons, like mean response rate, provides a signature of saccade preparation. However, the two signatures reflect complementary aspects of that preparation.


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