Gaze (eye-in-space) velocity-duration and velocity-amplitude curves were prepared for head-fixed and head-free gaze shifts in the rhesus monkey with an emphasis on large amplitudes. These plots revealed the presence of two distinct gaze reorientation mechanisms, one used when the gaze shift was small (less than 20 degrees) and the other utilized for large coordinated gaze shifts when the head was free. When head-free and head-fixed saccadic gaze shifts were compared in the same animal, no differences in the metrics were found for amplitudes less than 20 degrees. However, for large gaze shifts where contribution of the head to the change in gaze angle was considerable, head-free saccades were found to exhibit lower peak gaze velocities and greater durations than those recorded with the head-fixed paradigm. In order to differentiate between the eye saccades and combined saccadic eye-head gaze shifts, the latter have been termed gaze saccades. Change in head position and change in eye position were both measured during the actual gaze shift and were plotted against the gaze-shift amplitude to determine whether the head movement contributed significantly to the change in gaze angle. The results indicate that below 20 degrees the gaze shift is accomplished almost exclusively with the eyes and the head moves very little; however, for larger saccades, the head contributes approximately 80% of the total change in gaze angle with the eyes contributing only approximately 20%. Large saccadic eye-head gaze shifts do not exhibit 'bell-shaped' velocity profiles as do smaller head-fixed saccades; instead, gaze accelerates to reach a peak velocity after approximately 30-40 ms. This velocity is then maintained for the duration of the gaze shift. Close scrutiny of the fine structure of the velocity profiles of the eye, head, and gaze channels indicates that during gaze saccades, the eye and head movement motor programs interact to maintain gaze velocity nearly constant, unaffected by changes in head velocity. Previous authors had stated that when velocity-duration plots are obtained for oblique saccades of constant amplitude, the resulting points could be fitted with a hyperbolic function. These results were confirmed for head-free gaze saccades and extended to larger amplitudes. When an oblique saccade is made, the smaller component is stretched in duration to match the duration of the larger component. However, as the gaze shift becomes large (greater than 40 degrees), the relationship becomes more complex.(ABSTRACT TRUNCATED AT 400 WORDS)
The mechanisms of eye-head coordination were studied in two alert juvenile rhesus monkeys. Animals were trained to follow a target light to obtain a water reward and the combined eye-head gaze shifts in response to target steps with a variably sized horizontal components were studied. During a certain random portion of the gaze shifts, a torque motor was used to perturb the head to investigate the operational state of the vestibuloocular reflex (VOR) during the saccadic gaze shift. The effects of perturbing the head were assessed during five different conditions: horizontal target steps ranging from 10 to 80 degrees in amplitude; oblique target steps where the vertical component was larger than the horizontal component; purely vertical target steps 10-40 degrees in amplitude; both horizontal and oblique target steps delivered while the animals' saccades had been slowed by the use of diazepam; and large spontaneous gaze shifts in response to both sounds and visual stimuli. Comparison of perturbed and unperturbed large-amplitude (greater than 40 degrees) gaze shifts indicate that the VOR is turned off for most of the duration of the movement. Nonetheless, there is an apparent interaction between the saccadic eye movement and the head movement, thus, as the head velocity increases, the eye velocity decreases so that gaze velocity remains nearly constant throughout the gaze shift. Since the VOR is turned off when this interaction occurs, it must represent an interaction between the actual eye and head movement motor programs themselves. Although the results were not quite as clear for small saccades (less than 20 degrees), experiments on animals whose saccades had been slowed either by the use of diazepam or by combining a small horizontal component with a large vertical component indicate that the VOR is left on during these smaller gaze shifts. During quite small gaze shifts (less than 10 degrees), the VOR is clearly functioning; however, as the size of the gaze shift is increased, this becomes less clear, and there appears to be a region where the VOR operates with a gain substantially less than normal before it enters the large gaze shift region where the VOR is turned off entirely.(ABSTRACT TRUNCATED AT 400 WORDS)
The action potentials of single neurons were recorded extracellularly throughout the rostral vestibular nuclei and subadjacent reticular formation in three alert, juvenile, rhesus monkeys. Neuronal responses were tested during a) sinusoidal pitch oscillations in darkness, b) cancellation of the vestibuloocular reflex (VOR) during similar oscillations by fixation of a target moving with the head, c) sinusoidal vertical smooth pursuit, d) vertical saccades, and e) fixation with the head stationary. Eye movements were measured using the magnetic field-search coil technique. Of the 527 neurons isolated, 318 responded to pitch oscillation and/or vertical eye movements. The latter cells could be classified into six categories. Of this group, 273 cells were recorded from for sufficient time to allow them to be fully tested and form the basis of this report. Cells were classified as follows: pure-vestibular cells with firing rates modulated only by head velocity (15%), vestibular-pause cells that were similar to the pure-vestibular cells but paused for saccades in all directions (10%), gaze-velocity cells that modulated their rates in proportion to vertical eye velocity in space (7%), position cells with rates modulated by changes in eye position in the head but that did not burst or pause during saccades (33%), position-burst cells that also carried an eye-position signal but did burst during saccades in one direction and paused in the opposite direction (15%), and position-vestibular-pause cells that carried signals proportional to eye position in the head and head velocity and paused during all saccades (20%). Most cells that carried an eye-position signal also carried an eye-velocity signal during pursuit. Position and position-burst cells could be divided into two subcategories. Position cells that also reported head velocity represented 20% of the total sample, while those without head-velocity signals made up the remaining 13%. Position-burst cells were divided into two subcategories based on their behavior during pitch oscillation in darkness. Both carried eye-velocity signals during pursuit, but only one type (8% of the total sample) also carried an eye-velocity signal during vestibular eye movements in the dark, while the other (7%) did not. Some cells in all six categories except the pure-vestibular cells responded antidromically to stimulation of the medial longitudinal fasciculus (MLF). Only the position-vestibular-pause, position-burst, and gaze-velocity cells, however, were judged to be commonly antidromically activated, suggesting that these three cell types are the major contributors to the MLF from the rostral vestibular nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)
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)
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