scholarly journals Electrical Stimulation of the Supplementary Eye Fields in the Head-Free Macaque Evokes Kinematically Normal Gaze Shifts

2003 ◽  
Vol 89 (6) ◽  
pp. 2961-2974 ◽  
Author(s):  
Julio C. Martinez-Trujillo ◽  
Hongying Wang ◽  
J. Douglas Crawford

The supplementary eye fields (SEFs), located on the dorsomedial surface of the frontal cortex, are involved in high-level aspects of saccade generation. Some reports suggest that the same area could also be involved in the generation of motor commands for the head. If so, it is important to establish whether this structure encodes eye and head commands separately or gaze commands that give rise to coordinated eye-head movements. Here we systematically stimulated (50 μA, 300 Hz, 200 ms) the SEF of two head-free (head unrestrained) macaques while recording three-dimensional eye and head rotations. A total of 55 sites were found to consistently elicit saccade-like gaze movements, always in the contralateral direction with variable vertical components, and ranging in average amplitude from 5 to 60°. These movements were always a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between these movements and natural gaze shifts. The kinematics of the elicited movements (i.e., their temporal structure, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were indistinguishable from those of natural gaze shifts. Additionally, they obeyed the same three-dimensional constraints as natural gaze shifts (i.e., eye-in-head movements obeyed Listing's law, whereas head- and eye-in-space movements obeyed Donders' law). In summary, gaze movements evoked by stimulating the SEF were indistinguishable from natural coordinated eye-head gaze shifts. Based on this we conclude that the SEF explicitly encodes gaze and that the kinematics aspects of eye-head coordination are implicitly specified by mechanisms downstream from the SEF.

2010 ◽  
Vol 104 (6) ◽  
pp. 3462-3475 ◽  
Author(s):  
Jachin A. Monteon ◽  
Alina G. Constantin ◽  
Hongying Wang ◽  
Julio Martinez-Trujillo ◽  
J. Douglas Crawford

The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30–100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity–amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listing's law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listing's plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye–head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye–head coordination are likely specified by downstream mechanisms.


2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.


2007 ◽  
Vol 98 (2) ◽  
pp. 696-709 ◽  
Author(s):  
A. G. Constantin ◽  
H. Wang ◽  
J. C. Martinez-Trujillo ◽  
J. D. Crawford

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.


2012 ◽  
Vol 107 (6) ◽  
pp. 1694-1710 ◽  
Author(s):  
Brendan B. Chapman ◽  
Michael A. Pace ◽  
Sharon L. Cushing ◽  
Brian D. Corneil

The supplementary eye fields (SEF) are thought to enable higher-level aspects of oculomotor control. The goal of the present experiment was to learn more about the SEF's role in orienting, specifically by examining neck muscle recruitment evoked by stimulation of the SEF. Neck muscle activity was recorded from multiple muscles in two monkeys during SEF stimulation (100 μA, 150–300 ms, 300 Hz, with the head restrained or unrestrained) delivered 200 ms into a gap period, before a visually guided saccade initiated from a central position (doing so avoids confounds between initial position and prestimulation neck muscle activity). SEF stimulation occasionally evoked overt gaze shifts and/or head movements but almost always evoked a response that invariably consisted of a contralateral head turning synergy by increasing activity on contralateral turning muscles and decreasing activity on ipsilateral turning muscles (when background activity was present). Neck muscle responses began well in advance of evoked gaze shifts (∼30 ms after stimulation onset, leading gaze shifts by ∼40–70 ms on average), started earlier and attained a larger magnitude when accompanied by progressively larger gaze shifts, and persisted on trials without overt gaze shifts. The patterns of evoked neck muscle responses resembled those evoked by frontal eye field (FEF) stimulation, except that response latencies from the SEF were ∼10 ms longer. This basic description of the cephalomotor command evoked by SEF stimulation suggests that this structure, while further removed from the motor periphery than the FEF, accesses premotor orienting circuits in the brain stem and spinal cord in a similar manner.


1997 ◽  
Vol 77 (2) ◽  
pp. 654-666 ◽  
Author(s):  
Douglas Tweed

Tweed, Douglas. Three-dimensional model of the human eye-head saccadic system. J. Neurophysiol. 77: 654–666, 1997. Current theories of eye-head gaze shifts deal only with one-dimensional motion, and do not touch on three-dimensional (3-D) issues such as curvature and Donders' laws. I show that recent 3-D data can be explained by a model based on ideas that are well established from one-dimensional studies, with just one new assumption: that the eye is driven toward a 3-D orientation in space that has been chosen so that Listing's law of the eye in head will hold when the eye-head movement is complete. As in previous, one-dimensional models, the eye and head are feedback-guided and the commands specifying desired eye position eye pass through a neural “saturation” so as to stay within the effective oculomotor range. The model correctly predicts the complex, 3-D trajectories of the head, eye in space, and eye in head in a variety of saccade tasks. And when it moves repeatedly to the same target, varying the contributions of eye and head, the model lands in different eye-in-space positions, but these positions differ only in their cyclotorsion about the line of sight, so they all point that line at the target—a behavior also seen in real eye-head saccades. Between movements the model obeys Listing's law of the eye in head and Donders' law of the head on torso, but during certain gaze shifts involving large torsional head movements, it shows marked, 8° deviations from Listing's law. These deviations are the most important untested predictions of the theory. Their experimental refutation would sink the model, whereas confirmation would strongly support its central claim that the eye moves toward a 3-D position in space chosen to obey Listing's law and, therefore, that a Listing operator exists upstream from the eye pulse generator.


2007 ◽  
Vol 98 (1) ◽  
pp. 360-373 ◽  
Author(s):  
Neeraj J. Gandhi ◽  
David L. Sparks

Natural movements often include actions integrated across multiple effectors. Coordinated eye-head movements are driven by a command to shift the line of sight by a desired displacement vector. Yet because extraocular and neck motoneurons are separate entities, the gaze shift command must be separated into independent signals for eye and head movement control. We report that this separation occurs, at least partially, at or before the level of pontine omnipause neurons (OPNs). Stimulation of the OPNs prior to and during gaze shifts temporally decoupled the eye and head components by inhibiting gaze and eye saccades. In contrast, head movements were consistently initiated before gaze onset, and ongoing head movements continued along their trajectories, albeit with some characteristic modulations. After stimulation offset, a gaze shift composed of an eye saccade, and a reaccelerated head movement was produced to preserve gaze accuracy. We conclude that signals subject to OPN inhibition produce the eye-movement component of a coordinated eye-head gaze shift and are not the only signals involved in the generation of the head component of the gaze shift.


1995 ◽  
Vol 73 (2) ◽  
pp. 766-779 ◽  
Author(s):  
D. Tweed ◽  
B. Glenn ◽  
T. Vilis

1. Three-dimensional (3D) eye and head rotations were measured with the use of the magnetic search coil technique in six healthy human subjects as they made large gaze shifts. The aims of this study were 1) to see whether the kinematic rules that constrain eye and head orientations to two degrees of freedom between saccades also hold during movements; 2) to chart the curvature and looping in eye and head trajectories; and 3) to assess whether the timing and paths of eye and head movements are more compatible with a single gaze error command driving both movements, or with two different feedback loops. 2. Static orientations of the eye and head relative to space are known to resemble the distribution that would be generated by a Fick gimbal (a horizontal axis moving on a fixed vertical axis). We show that gaze point trajectories during eye-head gaze shifts fit the Fick gimbal pattern, with horizontal movements following straight "line of latitude" paths and vertical movements curving like lines of longitude. However, horizontal (and to a lesser extent vertical) movements showed direction-dependent looping, with rightward and leftward (and up and down) saccades tracing slightly different paths. Plots of facing direction (the analogue of gaze direction for the head) also showed the latitude/longitude pattern, without looping. In radial saccades, the gaze point initially moved more vertically than the target direction and then curved; head trajectories were straight. 3. The eye and head components of randomly sequenced gaze shifts were not time locked to one another. The head could start moving at any time from slightly before the eye until 200 ms after, and the standard deviation of this interval could be as large as 80 ms. The head continued moving for a long (up to 400 ms) and highly variable time after the gaze error had fallen to zero. For repeated saccades between the same targets, peak eye and head velocities were directly, but very weakly, correlated; fast eye movements could accompany slow head movements and vice versa. Peak head acceleration and deceleration were also very weakly correlated with eye velocity. Further, the head rotated about an essentially fixed axis, with a smooth bell-shaped velocity profile, whereas the axis of eye rotation relative to the head varied throughout the movement and the velocity profiles were more ragged. 4. Plots of 3D eye orientation revealed strong and consistent looping in eye trajectories relative to space.(ABSTRACT TRUNCATED AT 400 WORDS)


2009 ◽  
Vol 101 (4) ◽  
pp. 1730-1741 ◽  
Author(s):  
Vladimir Marlinski ◽  
Robert A. McCrea

Sixty vestibular nuclei neurons antidromically activated by electrical stimulation of the ventroposterior thalamus were recorded in two alert squirrel monkeys. The majority of these neurons were monosynaptically activated by vestibular nerve electrical stimulation. Forty-seven neurons responded to animal rotations around the earth-vertical axis; 16 of them also responded to translations in the horizontal plane. The mean sensitivity to 0.5-Hz rotations of 80°/s velocity was 0.40 ± 0.31 spikes·s−1·deg−1·s−1. Rotational responses were in phase with stimulus velocity. Sensitivities to 0.5-Hz translations of 0.1 g acceleration varied from 92.2 to 359 spikes·s−1· g−1 and response phases varied from 10.1° lead to −98° lag. The firing behavior in 28 neurons was studied during rotation of the whole animal, of the trunk, and voluntary and involuntary rotations of the head. Two classes of vestibulothalamic neurons were distinguished. One class of neurons generated signals related to movement of the head that were similar either when the head and trunk move together or when the head moves on the stationary trunk. A fraction of these neurons fired during involuntary head movements only. A second class of neurons generated signals related to movement of the trunk. They responded when the trunk moved alone or simultaneously with the head, but did not respond to head rotations while the trunk was stationary.


2008 ◽  
Vol 100 (2) ◽  
pp. 763-780 ◽  
Author(s):  
Yongqing Xiang ◽  
Sergei B. Yakushin ◽  
Mikhail Kunin ◽  
Theodore Raphan ◽  
Bernard Cohen

Little is known about the three-dimensional characteristics of vestibulocollic reflexes during natural locomotion. Here we determined how well head stability is maintained by the angular and linear vestibulocollic reflexes (aVCR, lVCR) during quadrupedal locomotion in rhesus and cynomolgus monkeys. Animals walked on a treadmill at velocities of 0.4–1.25 m/s. Head rotations were represented by Euler angles (Fick convention). The head oscillated in yaw and roll at stride frequencies (≈1–2 Hz) and pitched at step frequencies (≈2–4 Hz). Head angular accelerations (100–2,500°/s2) were sufficient to have excited the aVOR to stabilize gaze. Pitch and roll head movements were <7°, peak to peak, and the amplitude was unrelated to stride frequency. Yaw movements were larger due to spontaneous voluntary head shifts and were smaller at higher walking velocities. Head translations were small (≤4 cm). Cynomolgus monkeys positioned their heads more forward in pitch than the rhesus monkeys. None of the animals maintained a forward head fixation point, indicating that the lVCR contributed little to compensatory head movements in these experiments. Significantly, aVCR gains in roll and pitch were close to unity and phases were ≈180° over the full frequency range of natural walking, which is in contrast to previous findings using anesthesia or passive trunk rotation with body restraint. We conclude that the behavioral state associated with active body motion is necessary to maintain head stability in pitch and roll over the full range of stride/step frequencies encountered during walking.


2002 ◽  
Vol 88 (4) ◽  
pp. 1980-1999 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz

The role of the primate superior colliculus (SC) in orienting head movements was studied by recording electromyographic (EMG) activity from multiple neck muscles following electrical stimulation of the SC. Combining SC stimulation with neck EMG recordings provides an objective and sensitive measure of the SC drive onto neck muscle motoneurons, particularly in relation to evoked gaze shifts. In this paper, we address how neck EMG responses to SC stimulation in head-restrained monkeys depend on the rostrocaudal, mediolateral, and dorsoventral location of the stimulating electrode within the SC and vary with manipulations of the eye position prior to stimulation onset and changes in stimulation current and duration. Stimulation predominantly evoked EMG responses on the muscles obliquus capitis inferior, rectus capitis posterior major, and splenius capitis. These responses became larger in magnitude and shorter in onset latency for progressively more caudal stimulation locations, consistent with turning the head. However, evoked responses persisted even for more rostral stimulation locations usually not associated with head movements. Manipulating initial eye position revealed that the magnitude of evoked responses became stronger as the eyes attained positions contralateral to the side of stimulation, consistent with a summation between a generic command evoked by SC stimulation and the influence of eye position on tonic neck EMG. Manipulating stimulation current and duration revealed that the relationship between gaze shifts and evoked EMG responses is not obligatory: short-duration (<20 ms) or low-current stimulation evoked neck EMG responses in the absence of gaze shifts. However, long-duration stimulation (>150 ms) occasionally revealed a transient neck EMG response aligned on the onset of sequential gaze shifts. We conclude that the SC drive to neck muscle motoneurons is far more widespread than traditionally supposed and is relayed through intervening elements which may or may not be activated in association with gaze shifts.


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