Widespread Presaccadic Recruitment of Neck Muscles by Stimulation of the Primate Frontal Eye Fields

2007 ◽  
Vol 98 (3) ◽  
pp. 1333-1354 ◽  
Author(s):  
James K. Elsley ◽  
Benjamin Nagy ◽  
Sharon L. Cushing ◽  
Brian D. Corneil
Keyword(s):  
Neck Muscles ◽  
Head Movements ◽  
Emg Activity ◽  
Head Motion ◽  
Frontal Eye Fields ◽  
Conduction Time ◽  
Evoked Responses ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Stimulation Of

We studied the role of the primate frontal eye fields (FEFs) in eye-head gaze shifts by recording EMG activity from multiple dorsal neck muscles after electrical stimulation of a broad distribution of sites throughout FEF. We assess our results in light of four mechanisms forwarded to account for why eye and head movements follow FEF stimulation. Two mechanisms propose that movements are generated indirectly by FEF stimulation in response to either a percept or an eccentric orbital position. Two other mechanisms propose that movements are evoked directly through the issuance of either a gaze command or separate eye and head commands. FEF stimulation evoked short-latency (∼20 ms) neck EMG responses from the vast majority (>95%) of stimulation sites. Evoked responses usually preceded the gaze shift by ∼20 ms, even for small gaze shifts (<10°) not typically associated with head motion. Evoked responses began earlier and attained a larger magnitude when accompanied by larger gaze shifts and took a form consistent with the recruitment of the appropriately directed head movements to accompany the evoked gaze shift. We also observed robust neck EMG even when stimulation failed to evoke a gaze shift and occasionally observed head-only movements when the head was unrestrained. These results resemble neck EMG evoked from the superior colliculus (SC). Neck EMG response latencies approached the minimal conduction time to the motor periphery and hence are not consistent with either of the indirect mechanisms. The widespread nature of the cephalomotor drive from the FEF, the scaling of neck EMG responses with gaze magnitude, and the consistently earlier generation of the EMG versus gaze response are difficult to reconcile with suggestions that separate FEF channels encode eye and head motion independently. The most parsimonious interpretation is that a gaze command issued by the FEF is decomposed into eye and head commands downstream of the SC. The relative timing of the neck EMG and gaze shift responses, and the presence of neck EMG responses on trials without gaze shifts, implies that head premotor elements are not subjected to the same brain stem control mechanisms governing gaze shifts.

Neck Muscle Responses to Stimulation of Monkey Superior Colliculus. II. Gaze Shift Initiation and Volitional Head Movements

2002 ◽  
Vol 88 (4) ◽  
pp. 2000-2018 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz
Keyword(s):  
Superior Colliculus ◽  
Neck Muscles ◽  
Head Movements ◽  
Emg Activity ◽  
Neck Muscle ◽  
Gaze Shift ◽  
Antagonist Muscles ◽  
Agonist And Antagonist ◽  
Agonist And Antagonist Muscles ◽  
Stimulation Of

We report neck muscle activity and head movements evoked by electrical stimulation of the superior colliculus (SC) in head-unrestrained monkeys. Recording neck electromyography (EMG) circumvents complications arising from the head's inertia and the kinetics of muscle force generation and allows precise assessment of the neuromuscular drive to the head plant. This study served two main purposes. First, we sought to test the predictions made in the companion paper of a parallel drive from the SC onto neck muscles. Low-current, long-duration stimulation evoked both neck EMG responses and head movements either without or prior to gaze shifts, testifying to a SC drive to neck muscles that is independent of gaze-shift initiation. However, gaze-shift initiation was linked to a transient additional EMG response and head acceleration, confirming the presence of a SC drive to neck muscles that is dependent on gaze-shift initiation. We forward a conceptual neural architecture and suggest that this parallel drive provides the oculomotor system with the flexibility to orient the eyes and head independently or together, depending on the behavioral context. Second, we compared the EMG responses evoked by SC stimulation to those that accompanied volitional head movements. We found characteristic features in the underlying pattern of evoked neck EMG that were not observed during volitional head movements in spite of the seemingly natural kinematics of evoked head movements. These features included reciprocal patterning of EMG activity on the agonist and antagonist muscles during stimulation, a poststimulation increase in the activity of antagonist muscles, and synchronously evoked responses on agonist and antagonist muscles regardless of initial horizontal head position. These results demonstrate that the electrically evoked SC drive to the head cannot be considered as a neural replicate of the SC drive during volitional head movements and place important new constraints on the interpretation of electrically evoked head movements.

scholarly journals Neck Muscle Responses to Stimulation of Monkey Superior Colliculus. I. Topography and Manipulation of Stimulation Parameters

2002 ◽  
Vol 88 (4) ◽  
pp. 1980-1999 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Douglas P. Munoz
Keyword(s):  
Superior Colliculus ◽  
Head Movements ◽  
Emg Activity ◽  
Eye Position ◽  
Neck Muscle ◽  
Evoked Responses ◽  
Inferior Rectus ◽  
Gaze Shifts ◽  
Stimulation Current ◽  
Stimulation Of

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.

scholarly journals Electrical Stimulation of the Frontal Eye Field in a Monkey Produces Combined Eye and Head Movements

2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Eye Field ◽  
A Site ◽  
Head Rotations ◽  
Stimulation Of

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.

scholarly journals Dissociation of Eye and Head Components of Gaze Shifts by Stimulation of the Omnipause Neuron Region

2007 ◽  
Vol 98 (1) ◽  
pp. 360-373 ◽  
Author(s):  
Neeraj J. Gandhi ◽  
David L. Sparks
Keyword(s):  
Head Movement ◽  
Displacement Vector ◽  
Movement Control ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Movement Component ◽  
Neck Motoneurons ◽  
Stimulation Of

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.

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.

Neck Muscles in the Rhesus Monkey. II. Electromyographic Patterns of Activation Underlying Postures and Movements

2001 ◽  
Vol 86 (4) ◽  
pp. 1729-1749 ◽  
Author(s):  
Brian D. Corneil ◽  
Etienne Olivier ◽  
Frances J. R. Richmond ◽  
Gerald E. Loeb ◽  
Douglas P. Munoz
Keyword(s):  
Muscle Activation ◽  
Neck Muscles ◽  
Head Movements ◽  
Emg Activity ◽  
Neck Muscle ◽  
Spatial And Temporal Patterns ◽  
Gaze Shifts ◽  
Antagonist Muscles ◽  
Agonist And Antagonist ◽  
Head Positions

Electromyographic (EMG) activity was recorded in ≤12 neck muscles in four alert monkeys whose heads were unrestrained to describe the spatial and temporal patterns of neck muscle activation accompanying a large range of head postures and movements. Some head postures and movements were elicited by training animals to generate gaze shifts to visual targets. Other spontaneous head movements were made during orienting, tracking, feeding, expressive, and head-shaking behaviors. These latter movements exhibited a wider range of kinematic patterns. Stable postures and small head movements of only a few degrees were associated with activation of a small number of muscles in a reproducible synergy. Additional muscles were recruited for more eccentric postures and larger movements. For head movements during trained gaze shifts, movement amplitude, velocity, and acceleration were correlated linearly and agonist muscles were recruited without antagonist muscles. Complex sequences of reciprocal bursts in agonist and antagonist muscles were observed during very brisk movements. Turning movements of similar amplitudes that began from different initial head positions were associated with systematic variations in the activities of different muscles and in the relative timings of these activities. Unique recruitment synergies were observed during feeding and head-shaking behaviors. Our results emphasize that the recruitment of a given muscle was generally ordered and consistent but that strategies for coordination among various neck muscles were often complex and appeared to depend on the specifics of musculoskeletal architecture, posture, and movement kinematics that differ substantially among species.

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.

Rapid horizontal gaze movement in the monkey

1995 ◽  
Vol 73 (4) ◽  
pp. 1632-1652 ◽  
Author(s):  
J. O. Phillips ◽  
L. Ling ◽  
A. F. Fuchs ◽  
C. Siebold ◽  
J. J. Plorde
Keyword(s):  
Eye Movement ◽  
Head Movement ◽  
Vertical Axis ◽  
Head Position ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Small Correction ◽  
Horizontal Gaze

1. We studied horizontal eye and head movements in three monkeys that were trained to direct their gaze (eye position in space) toward jumping targets while their heads were both fixed and free to rotate about a vertical axis. We considered all gaze movements that traveled > or = 80% of the distance to the new visual target. 2. The relative contributions and metrics of eye and head movements to the gaze shift varied considerably from animal to animal and even within animals. Head movements could be initiated early or late and could be large or small. The eye movements of some monkeys showed a consistent decrease in velocity as the head accelerated, whereas others did not. Although all gaze shifts were hypometric, they were more hypometric in some monkeys than in others. Nevertheless, certain features of the gaze shift were identifiable in all monkeys. To identify those we analyzed gaze, eye in head position, and head position, and their velocities at three points in time during the gaze shift: 1) when the eye had completed its initial rotation toward the target, 2) when the initial gaze shift had landed, and 3) when the head movement was finished. 3. For small gaze shifts (< 20 degrees) the initial gaze movement consisted entirely of an eye movement because the head did not move. As gaze shifts became larger, the eye movement contribution saturated at approximately 30 degrees and the head movement contributed increasingly to the initial gaze movement. For the largest gaze shifts, the eye usually began counterrolling or remained stable in the orbit before gaze landed. During the interval between eye and gaze end, the head alone carried gaze to completion. Finally, when the head movement landed, it was almost aimed at the target and the eye had returned to within 10 +/- 7 degrees, mean +/- SD, of straight ahead. Between the end of the gaze shift and the end of the head movement, gaze remained stable in space or a small correction saccade occurred. 4. Gaze movements < 20 degrees landed accurately on target whether the head was fixed or free. For larger target movements, both head-free and head-fixed gaze shifts became increasingly hypometric. Head-free gaze shifts were more accurate, on average, but also more variable. This suggests that gaze is controlled in a different way with the head free. For target amplitudes < 60 degrees, head position was hypometric but the error was rather constant at approximately 10 degrees.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Target modality determines eye-head coordination in nonhuman primates: implications for gaze control

2011 ◽  
Vol 106 (4) ◽  
pp. 2000-2011 ◽  
Author(s):  
Luis C. Populin ◽  
Abigail Z. Rajala
Keyword(s):  
Nonhuman Primates ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Midbrain Structure ◽  
The Subject ◽  
Visual Targets ◽  
Time Of Presentation

We have studied eye-head coordination in nonhuman primates with acoustic targets after finding that they are unable to make accurate saccadic eye movements to targets of this type with the head restrained. Three male macaque monkeys with experience in localizing sounds for rewards by pointing their gaze to the perceived location of sources served as subjects. Visual targets were used as controls. The experimental sessions were configured to minimize the chances that the subject would be able to predict the modality of the target as well as its location and time of presentation. The data show that eye and head movements are coordinated differently to generate gaze shifts to acoustic targets. Chiefly, the head invariably started to move before the eye and contributed more to the gaze shift. These differences were more striking for gaze shifts of <20–25° in amplitude, to which the head contributes very little or not at all when the target is visual. Thus acoustic and visual targets trigger gaze shifts with different eye-head coordination. This, coupled to the fact that anatomic evidence involves the superior colliculus as the link between auditory spatial processing and the motor system, suggests that separate signals are likely generated within this midbrain structure.

Brain Stem Omnipause Neurons and the Control of CombinedEye-Head Gaze Saccades in the Alert Cat

1998 ◽  
Vol 79 (6) ◽  
pp. 3060-3076 ◽  
Author(s):  
Martin Paré ◽  
Daniel Guitton
Keyword(s):  
Gaze Control ◽  
Error Signal ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Alert Cat ◽  
Motor Error ◽  
Omnipause Neurons ◽  
Gaze Saccades ◽  
Stimulation Of

Paré, Martin and Daniel Guitton. Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. J. Neurophysiol. 79: 3060–3076, 1998. When the head is unrestrained, rapid displacements of the visual axis—gaze shifts (eye-re-space)—are made by coordinated movements of the eyes (eye-re-head) and head (head-re-space). To address the problem of the neural control of gaze shifts, we studied and contrasted the discharges of omnipause neurons (OPNs) during a variety of combined eye-head gaze shifts and head-fixed eye saccades executed by alert cats. OPNs discharged tonically during intersaccadic intervals and at a reduced level during slow perisaccadic gaze movements sometimes accompanying saccades. Their activity ceased for the duration of the saccadic gaze shifts the animal executed, either by head-fixed eye saccades alone or by combined eye-head movements. This was true for all types of gaze shifts studied: active movements to visual targets; passive movements induced by whole-body rotation or by head rotation about stationary body; and electrically evoked movements by stimulation of the caudal part of the superior colliculus (SC), a central structure for gaze control. For combined eye-head gaze shifts, the OPN pause was therefore not correlated to the eye-in-head trajectory. For instance, in active gaze movements, the end of the pause was better correlated with the gaze end than with either the eye saccade end or the time of eye counterrotation. The hypothesis that cat OPNs participate in controlling gaze shifts is supported by these results, and also by the observation that the movements of both the eyes and the head were transiently interrupted by stimulation of OPNs during gaze shifts. However, we found that the OPN pause could be dissociated from the gaze-motor-error signal producing the gaze shift. First, OPNs resumed discharging when perturbation of head motion briefly interrupted a gaze shift before its intended amplitude was attained. Second, stimulation of caudal SC sites in head-free cat elicited large head-free gaze shifts consistent with the creation of a large gaze-motor-error signal. However, stimulation of the same sites in head-fixed cat produced small “goal-directed” eye saccades, and OPNs paused only for the duration of the latter; neither a pause nor an eye movement occurred when the same stimulation was applied with the eyes at the goal location. We conclude that OPNs can be controlled by neither a simple eye control system nor an absolute gaze control system. Our data cannot be accounted for by existing models describing the control of combined eye-head gaze shifts and therefore put new constraints on future models, which will have to incorporate all the various signals that act synergistically to control gaze shifts.

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