In Multiple-Step Gaze Shifts: Omnipause (OPNs) and Collicular Fixation Neurons Encode Gaze Position Error; OPNs Gate Saccades

2002 ◽  
Vol 88 (4) ◽  
pp. 1726-1742 ◽  
Author(s):  
André Bergeron ◽  
Daniel Guitton
Keyword(s):  
Superior Colliculus ◽  
Firing Frequency ◽  
Position Error ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Saccade ◽  
Saccade Onset ◽  
Gaze Position ◽  
Gaze Saccades ◽  
Multiple Step

The superior colliculus (SC), via its projections to the pons, is a critical structure for driving rapid orienting movements of the visual axis, called gaze saccades, composed of coordinated eye-head movements. The SC contains a motor map that encodes small saccade vectors rostrally and large ones caudally. A zone in the rostral pole may have a different function. It contains superior colliculus fixation neurons (SCFNs) with probable projections to omnipause neurons (OPNs) of the pons. SCFNs and OPNs discharge tonically during visual fixation and pause during single-step gaze saccades. The OPN tonic discharge inhibits saccades and its cessation (pause) permits saccade generation. We have proposed that SCFNs control the OPN discharge. We compared the discharges of SCFNs and OPNs recorded while cats oriented horizontally, to the left and right, in the dark to a remembered target. Cats used multiple-step gaze shifts composed of a series of small gaze saccades, of variable amplitude and number, separated by periods of variable duration (plateaus) in which gaze was immobile or moving at low velocity (<25°/s). Just after contralaterally (ipsilaterally) presented targets, the firing frequency of SCFNs decreased to almost zero (remained constant at background). As multiple-step gaze shifts progressed in either direction in the dark, these activity levels prevailed until the distance between gaze and target [gaze position error (GPE)] reached ∼16°. At this point, firing frequency gradually increased, without saccade-related pauses, until a maximum was reached when gaze arrived on target location (GPE = 0°). SCFN firing frequency encoded GPE; activity was not correlated to characteristics or occurrence of gaze saccades. By comparison, after target presentation to left or right, OPN activity remained steady at pretarget background until first gaze saccade onset, during which activity paused. During the first plateau, activity resumed at a level lower than background and continued at this level during subsequent plateaus until GPE ∼8° was reached. As GPE decreased further, tonic activity during plateaus gradually increased until a maximum (greater than background) was reached when gaze was on goal (GPE = 0°). OPNs, like SCFNs, encoded GPE, but they paused during every gaze saccade, thereby revealing, unlike for SCFNs, strong coupling to motor events. The firing frequency increase in SCFNs as GPE decreased, irrespective of trajectory characteristics, implies these cells get feedback on GPE, which they may communicate to OPNs. We hypothesize that at the end of a gaze-step sequence, impulses from SCFNs onto OPNs may suppress further movements away from the target.

Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades

1990 ◽  
Vol 64 (6) ◽  
pp. 1873-1891 ◽  
Author(s):  
R. D. Tomlinson
Keyword(s):  
Head Movement ◽  
Head Movements ◽  
Whole Body ◽  
Midsagittal Plane ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Gaze Stability ◽  
Gaze Saccade ◽  
Gaze Saccades

1. The behavior of the combined eye-head gaze saccade mechanism was investigated in the rhesus monkey under both normal circumstances and in the presence of perturbations delivered to the head by a torque motor. Animals were trained to follow a target light that stepped at regular intervals through an angle of 68 degrees (+/- 34 degrees with respect to the midsagittal plane). Thus all primary saccades were center crossing. On randomly occurring trials the torque motor was pulsed so as to perturb the trajectory of the head, thus allowing us to assess both the functional state of the vestibuloocular reflex (VOR) and the effects of such perturbations on gaze saccade accuracy (gaze is defined as the sum of eye-in-head plus head-in-space, and a gaze saccade as a combined eye-head saccadic gaze shift). 2. Gaze shifts can be divided into two discrete sections: the portion during which the gaze angle is changing (the saccadic portion), and the portion during which the gaze is stationary but the head continues to move (the terminal head-movement portion). For the system to accurately acquire eccentric targets, at least two criteria must be met: 1) the saccadic portion must be accurate, and 2) the compensatory eye movement that occurs during the terminal head-movement portion must be equal and opposite to the head movement, thereby maintaining gaze stability. Perturbations delivered during the terminal head-movement portion of the gaze shift indicated that VOR was functioning normally, and thus we concluded that the compensatory eye movements that accompany head movements were vestibular in origin. 3. As reported previously, during the saccadic portion of large-amplitude gaze saccades, the VOR ceases to function. In spite of this observation, the accuracy of the gaze saccade is not affected by perturbations delivered to the head. Gaze accuracy is maintained both by changing the duration of the saccadic portion and by altering the head trajectory. 4. Because rhesus monkeys often make very rapid head movements (1,200 degrees/s), we wished to discover the velocity range over which the monkey VOR might be expected to operate. Accordingly, in a second series of experiments, VOR function was assessed during passive whole-body rotations with the head fixed. By the use of spring-assisted manual rotations, peak velocities up to 850 degrees/s were achieved. When VOR gain was measured during such rotations, it was found to be equal to 0.9 up to the maximum velocities used.(ABSTRACT TRUNCATED AT 400 WORDS)

Visual-Vestibular Interaction Hypothesis for the Control of Orienting Gaze Shifts by Brain Stem Omnipause Neurons

2007 ◽  
Vol 97 (2) ◽  
pp. 1149-1162 ◽  
Author(s):  
Mario Prsa ◽  
Henrietta L. Galiana
Keyword(s):  
Brain Stem ◽  
Head Movements ◽  
Gaze Control ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Switching Mechanism ◽  
Interaction Hypothesis ◽  
Visual Vestibular Interaction ◽  
Motor Error ◽  
Gaze Position

Models of combined eye-head gaze shifts all aim to realistically simulate behaviorally observed movement dynamics. One of the most problematic features of such models is their inability to determine when a saccadic gaze shift should be initiated and when it should be ended. This is commonly referred to as the switching mechanism mediated by omni-directional pause neurons (OPNs) in the brain stem. Proposed switching strategies implemented in existing gaze control models all rely on a sensory error between instantaneous gaze position and the spatial target. Accordingly, gaze saccades are initiated after presentation of an eccentric visual target and subsequently terminated when an internal estimate of gaze position becomes nearly equal to that of the target. Based on behavioral observations, we demonstrate that such a switching mechanism is insufficient and is unable to explain certain types of movements. We propose an improved hypothesis for how the OPNs control gaze shifts based on a visual-vestibular interaction of signals known to be carried on anatomical projections to the OPN area. The approach is justified by the analysis of recorded gaze shifts interrupted by a head brake in animal subjects and is demonstrated by implementing the switching mechanism in an anatomically based gaze control model. Simulated performance reveals that a weighted sum of three signals: gaze motor error, head velocity, and eye velocity, hypothesized as inputs to OPNs, successfully reproduces diverse behaviorally observed eye-head movements that no other existing model can account for.

scholarly journals Role of the Primate Superior Colliculus in the Control of Head Movements

2007 ◽  
Vol 98 (4) ◽  
pp. 2022-2037 ◽  
Author(s):  
Mark M. G. Walton ◽  
Bernard Bechara ◽  
Neeraj J. Gandhi
Keyword(s):  
Superior Colliculus ◽  
Firing Rate ◽  
Head Movements ◽  
Neural Basis ◽  
Average Firing Rate ◽  
Gaze Shifts ◽  
Burst Neurons ◽  
The Gaze ◽  
Head Displacement ◽  
Elevated Frequency

One important behavioral role for head movements is to assist in the redirection of gaze. However, primates also frequently make head movements that do not involve changes in the line of sight. Virtually nothing is known about the neural basis of these head-only movements. In the present study, single-unit extracellular activity was recorded from the superior colliculus while monkeys performed behavioral tasks that permit the temporal dissociation of gaze shifts and head movements. We sought to determine whether superior colliculus contains neurons that modulate their activity in association with head movements in the absence of gaze shifts and whether classic gaze-related burst neurons also discharge for head-only movements. For 26% of the neurons in our sample, significant changes in average firing rate could be attributed to head-only movements. Most of these increased their firing rate immediately prior to the onset of a head movement and continued to discharge at elevated frequency until the offset of the movement. Others discharged at a tonic rate when the head was stable and decreased their activity, or paused, during head movements. For many putative head cells, average firing rate was found to be predictive of head displacement. Some neurons exhibited significant changes in activity associated with gaze, eye-only, and head-only movements, although none of the gaze-related burst neurons significantly modulated its activity in association with head-only movements. These results suggest the possibility that the superior colliculus plays a role in the control of head movements independent of gaze shifts.

scholarly journals Differential Influence of Attention on Gaze and Head Movements

2009 ◽  
Vol 101 (1) ◽  
pp. 198-206 ◽  
Author(s):  
Aarlenne Z. Khan ◽  
Gunnar Blohm ◽  
Robert M. McPeek ◽  
Philippe Lefèvre
Keyword(s):  
Reaction Times ◽  
Stimulus Onset ◽  
Head Movements ◽  
Neck Muscle ◽  
Gaze Shifts ◽  
Opposite Pattern ◽  
Saccade Onset ◽  
Highly Correlated ◽  
Onset Asynchrony ◽  
Electromyographic Signals

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye–head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye–head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye–head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.

Cerebellar contribution to the spatial encoding of orienting gaze shifts in the head-free cat

1994 ◽  
Vol 72 (5) ◽  
pp. 2547-2550 ◽  
Author(s):  
L. Goffart ◽  
D. Pelisson
Keyword(s):  
Constant Error ◽  
Visual Target ◽  
Fastigial Nucleus ◽  
Caudal Part ◽  
Gaze Shifts ◽  
Neural Processes ◽  
Correct Execution ◽  
Gaze Position ◽  
Gaze Saccades ◽  
Saccadic Dysmetria

1. Cerebellar saccadic dysmetria may result from a disturbance in the processes that ensure correct execution of gaze displacement. Alternatively, an impairment in the preparatory processes that lead to the specification of the movement goal may also produce this deficit. 2. We report here on a pharmacologically induced dysmetria that suggests a cerebellar contribution to the neural processes encoding the location of the goal for orienting gaze shifts. 3. Shifts of gaze (eye-in-space) were recorded in the head-free cat after the GABA agonist muscimol was unilaterally injected into the caudal part of the fastigial nucleus. 4. Gaze saccades towards the inactivated side were hypermetric. These ipsiversive movements overshot the target by a constant error, regardless of target eccentricity and initial gaze position. 5. Gaze saccades directed away from the inactivated side undershot the target. The degree of hypometria increased when the amplitude of the required movement increased. 6. These results suggest a different contribution of the caudal fastigial nucleus to the accuracy of visually triggered gaze shifts, depending on the direction of the impending saccade. The systematic error of ipsiversive movements and the inappropriate movements evoked by presenting a target at the same physical location as gaze reveal that fastigial inactivation interfered with the processes that encode the location of a visual target.

scholarly journals Frames of Reference for Gaze Saccades Evoked During Stimulation of Lateral Intraparietal Cortex

2007 ◽  
Vol 98 (2) ◽  
pp. 696-709 ◽  
Author(s):  
A. G. Constantin ◽  
H. Wang ◽  
J. C. Martinez-Trujillo ◽  
J. D. Crawford
Keyword(s):  
Three Dimensional ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Lateral Intraparietal Cortex ◽  
The Gaze ◽  
The Right ◽  
Gaze Position ◽  
Stimulation Of

Previous studies suggest that stimulation of lateral intraparietal cortex (LIP) evokes saccadic eye movements toward eye- or head-fixed goals, whereas most single-unit studies suggest that LIP uses an eye-fixed frame with eye-position modulations. The goal of our study was to determine the reference frame for gaze shifts evoked during LIP stimulation in head-unrestrained monkeys. Two macaques ( M1 and M2) were implanted with recording chambers over the right intraparietal sulcus and with search coils for recording three-dimensional eye and head movements. The LIP region was microstimulated using pulse trains of 300 Hz, 100–150 μA, and 200 ms. Eighty-five putative LIP sites in M1 and 194 putative sites in M2 were used in our quantitative analysis throughout this study. Average amplitude of the stimulation-evoked gaze shifts was 8.67° for M1 and 7.97° for M2 with very small head movements. When these gaze-shift trajectories were rotated into three coordinate frames (eye, head, and body), gaze endpoint distribution for all sites was most convergent to a common point when plotted in eye coordinates. Across all sites, the eye-centered model provided a significantly better fit compared with the head, body, or fixed-vector models (where the latter model signifies no modulation of the gaze trajectory as a function of initial gaze position). Moreover, the probability of evoking a gaze shift from any one particular position was modulated by the current gaze direction (independent of saccade direction). These results provide causal evidence that the motor commands from LIP encode gaze command in eye-fixed coordinates but are also subtly modulated by initial gaze position.

scholarly journals Activity of Cells in the Deeper Layers of the Superior Colliculus of the Rhesus Monkey: Evidence for a Gaze Displacement Command

1997 ◽  
Vol 78 (3) ◽  
pp. 1669-1690 ◽  
Author(s):  
Edward G. Freedman ◽  
David L. Sparks
Keyword(s):  
Eye Movements ◽  
Rhesus Monkey ◽  
Superior Colliculus ◽  
Single Cells ◽  
Head Movements ◽  
Gaze Shifts ◽  
Unit Recording ◽  
The Gaze ◽  
Head Displacement ◽  
Separate Channel

Freedman, Edward G. and David L. Sparks. Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: evidence for a gaze displacement command. J. Neurophysiol. 78: 1669–1690, 1997. When the head is free to move, microstimulation of the primate superior colliculus (SC) evokes coordinated movements of the eyes and head. The similarity between these stimulation-induced movements and visually guided movements indicates that the SC of the primate is involved in redirecting the line of sight (gaze). To determine how movement commands are represented by individual collicular neurons, we recorded the activity of single cells in the deeper layers of the superior colliculus of the rhesus monkey during coordinated eye-head gaze shifts. Two alternative hypotheses were tested. The “separate channel” hypothesis states that two displacement commands are generated by the SC: one signal specifying the amplitude and direction of eye movements and a second signal specifying the amplitude and direction of head movements. Alternatively, a single gaze displacement command could be generated by the SC (“gaze displacement” hypothesis). The activity of collicular neurons was examined during three behavioral dissociations of gaze, eye, and head movement amplitude and direction (metrics). Subsets of trials were selected in which the amplitude and direction of either gaze shifts or eye movements or head movements were relatively constant but the metrics of the other two varied over wide ranges. Under these conditions, the separate channel and gaze displacement hypotheses make differential predictions about the patterns of SC activity. We tested these differential predictions by comparing observed patterns with predicted patterns of neuronal activity. We obtained data consistent with the predictions of the gaze displacement hypothesis. The predictions of the separate channel hypothesis were not confirmed. Thus microstimulation data, single-unit recording data, and behavioral data are all consistent with the gaze displacement hypothesis of collicular function—the hypothesis that a gaze displacement signal is derived from the locus of activity within the motor map of the SC and subsequently is decomposed into separate eye and head displacement signals downstream from the colliculus.

Difference Between Visually and Electrically Evoked Gaze Saccades Disclosed by Altering the Head Moment of Inertia

2000 ◽  
Vol 83 (2) ◽  
pp. 1103-1107 ◽  
Author(s):  
Alexandre J. F. Coimbra ◽  
Philippe Lefèvre ◽  
Marcus Missal ◽  
Etienne Olivier
Keyword(s):  
Head Movements ◽  
Moment Of Inertia ◽  
Gaze Shifts ◽  
Feedback Information ◽  
Slowing Down ◽  
Movement Dynamics ◽  
On Line ◽  
Gaze Saccades ◽  
Visually Evoked Saccades

Differences between gaze shifts evoked by collicular electrical stimulation and those triggered by the presentation of a visual stimulus were studied in head-free cats by increasing the head moment of inertia. This maneuver modified the dynamics of these two types of gaze shifts by slowing down head movements. Such an increase in the head moment of inertia did not affect the metrics of visually evoked gaze saccades because their duration was precisely adjusted to compensate for these changes in movement dynamics. In contrast, the duration of electrically evoked gaze shifts remained constant irrespective of the head moment of inertia, and therefore their amplitude was significantly reduced. These results suggest that visually and electrically evoked gaze saccades are controlled by different mechanisms. Whereas the accuracy of visually evoked saccades is likely to be assured by on-line feedback information, the absence of duration adjustment in electrically evoked gaze shifts suggests that feedback information necessary to maintain their metrics is not accessible or is corrupted during collicular stimulation. This is of great importance when these two types of movements are compared to infer the role of the superior colliculus in the control of orienting gaze shifts.

scholarly journals Effect of Reversible Inactivation of Superior Colliculus on Head Movements

2008 ◽  
Vol 99 (5) ◽  
pp. 2479-2495 ◽  
Author(s):  
Mark M. G. Walton ◽  
Bernard Bechara ◽  
Neeraj J. Gandhi
Keyword(s):  
Superior Colliculus ◽  
Reaction Times ◽  
Movement Control ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Reversible Inactivation ◽  
The Gaze ◽  
Made In

Because of limitations in the oculomotor range, many gaze shifts must be accomplished using coordinated movements of the eyes and head. Stimulation and recording data have implicated the primate superior colliculus (SC) in the control of these gaze shifts. The precise role of this structure in head movement control, however, is not known. The present study uses reversible inactivation to gain insight into the role of this structure in the control of head movements, including those that accompany gaze shifts and those that occur in the absence of a change in gaze. Forty-five lidocaine injections were made in two monkeys that had been trained on a series of behavioral tasks that dissociate movements of the eyes and head. Reversible inactivation resulted in clear impairments in the animals’ ability to perform gaze shifts, manifested by increased reaction times, lower peak velocities, and increased durations. In contrast, comparable effects were not found for head movements (with or without gaze shifts) with the exception of a very small increase in reaction times of head movements associated with gaze shifts. Eye-head coordination was clearly affected by the injections with gaze onset occurring relatively later with respect to head onset. Following the injections, the head contributed slightly more to the gaze shift. These results suggest that head movements (with and without gaze shifts) can be controlled by pathways that do not involve SC.

Human Head-Free Gaze Saccades to Targets Flashed Before Gaze-Pursuit Are Spatially Accurate

1998 ◽  
Vol 80 (5) ◽  
pp. 2785-2789 ◽  
Author(s):  
Troy M. Herter ◽  
Daniel Guitton
Keyword(s):  
Motor System ◽  
Human Subjects ◽  
Human Head ◽  
Horizontal Meridian ◽  
Visual Axis ◽  
Saccade Onset ◽  
On Line ◽  
Saccade Task ◽  
Gaze Position ◽  
Gaze Saccades

Herter, Troy M. and Daniel Guitton. Human head-free gaze saccades to targets flashed before gaze-pursuit are spatially accurate. J. Neurophysiol. 80: 2785–2789, 1998. Previous studies have shown that accurate saccades can be generated, in the dark, that compensate for movements of the visual axis that result from movements of either the eyes alone or the head alone that intervene between target presentation and saccade onset. We have carried out experiments with human subjects to test whether gaze saccades (gaze = eye-in-space = eye-in-head + head-in-space) can be generated that compensate for smooth pursuit movements of gaze that intervene between target onset and gaze-saccade onset. In both head-unrestrained (head-free) and -restrained (head-fixed) conditions, subjects were asked to make gaze shifts, in the dark, to the remembered location of a briefly flashed target. On most trials, during the memory period, the subjects carried out intervening head-free gaze pursuit or head-fixed ocular pursuit along the horizontal meridian. On the remaining (control) trials, subjects did not carry out intervening pursuit movements during the memory period; this was the classical memory-guided saccade task. We found that the subjects accurately compensated for intervening movements of the visual axis in both the head-free and head-fixed conditions. We conclude that the human gaze-motor system is able to monitor on-line changes in gaze position and add them to initial retinal error, to program spatially accurate gaze saccades.

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