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 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.

Gaze-related activity of putative inhibitory burst neurons in the head-free cat

1993 ◽  
Vol 70 (6) ◽  
pp. 2678-2683 ◽  
Author(s):  
K. E. Cullen ◽  
D. Guitton ◽  
C. G. Rey ◽  
W. Jiang
Keyword(s):  
The Body ◽  
Head Movements ◽  
Related Activity ◽  
Visual Axis ◽  
Abducens Nucleus ◽  
Gaze Shifts ◽  
Burst Neurons ◽  
The Gaze ◽  
Output Neurons ◽  
The Relationship

1. Previous studies in the cat have demonstrated that output neurons of the superior collicular as well as brain stem omnipause neurons have discharges that are best correlated, not with the trajectory of the eye in the head but, with the trajectory of the visual axis in space (gaze = eye-in-head + head-in-space) during rapid orienting coordinated eye and head movements. In this study, we describe the gaze-related activity of cat premotor “inhibitory burst neurons”(IBNs) identified on the basis of their position relative to the abducens nucleus. 2. The firing behavior of IBNs was studied during 1) saccades made with the head stationary, 2) active orienting combined eye-head gaze shifts, and 3) passive movements of the head on the body. IBN discharges were well correlated with the duration and amplitude of saccades made when the head was stationary. In both head-free paradigms, the behavior of cat IBNs differed from that of previously described primate “saccade bursters”. The duration of their burst was better correlated with gaze than saccade duration, and the total number of spikes in a burst was well correlated with gaze amplitude and generally poorly correlated with saccade amplitude. The behavior of cat IBNs also differed from that of previously described primate “gaze bursters”. The slope of the relationship between the total number of spikes and gaze amplitude observed during head-free gaze shifts was significantly lower than that observed during head-fixed saccades. 3. These studies suggest that cat IBNs do not fit into the categories of gaze-bursters or saccade-bursters that have been described in primate studies.(ABSTRACT TRUNCATED AT 250 WORDS)

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.

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)

Sound-Localization Performance in the Cat: The Effect of Restraining the Head

2005 ◽  
Vol 93 (3) ◽  
pp. 1223-1234 ◽  
Author(s):  
Daniel J. Tollin ◽  
Luis C. Populin ◽  
Jordan M. Moore ◽  
Janet L. Ruhland ◽  
Tom C. T. Yin
Keyword(s):  
Short Duration ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Gaze Shifts ◽  
Localization Accuracy ◽  
Head Restraint ◽  
The Gaze ◽  
Long Duration ◽  
Localization Performance ◽  
Visual Targets

In oculomotor research, there are two common methods by which the apparent location of visual and/or auditory targets are measured, saccadic eye movements with the head restrained and gaze shifts (combined saccades and head movements) with the head unrestrained. Because cats have a small oculomotor range (approximately ±25°), head movements are necessary when orienting to targets at the extremes of or outside this range. Here we tested the hypothesis that the accuracy of localizing auditory and visual targets using more ethologically natural head-unrestrained gaze shifts would be superior to head-restrained eye saccades. The effect of stimulus duration on localization accuracy was also investigated. Three cats were trained using operant conditioning with their heads initially restrained to indicate the location of auditory and visual targets via eye position. Long-duration visual targets were localized accurately with little error, but the locations of short-duration visual and both long- and short-duration auditory targets were markedly underestimated. With the head unrestrained, localization accuracy improved substantially for all stimuli and all durations. While the improvement for long-duration stimuli with the head unrestrained might be expected given that dynamic sensory cues were available during the gaze shifts and the lack of a memory component, surprisingly, the improvement was greatest for the auditory and visual stimuli with the shortest durations, where the stimuli were extinguished prior to the onset of the eye or head movement. The underestimation of auditory targets with the head restrained is explained in terms of the unnatural sensorimotor conditions that likely result during head restraint.

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.

scholarly journals Matching the Oculomotor Drive During Head-Restrained and Head-Unrestrained Gaze Shifts in Monkey

2010 ◽  
Vol 104 (2) ◽  
pp. 811-828 ◽  
Author(s):  
Bernard P. Bechara ◽  
Neeraj J. Gandhi
Keyword(s):  
Mean Squared Error ◽  
Vestibular Nuclei ◽  
Cell Types ◽  
Head Movements ◽  
Abducens Nucleus ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Head Velocity ◽  
Burst Neurons ◽  
Eye Velocity

High-frequency burst neurons in the pons provide the eye velocity command (equivalently, the primary oculomotor drive) to the abducens nucleus for generation of the horizontal component of both head-restrained (HR) and head-unrestrained (HU) gaze shifts. We sought to characterize how gaze and its eye-in-head component differ when an “identical” oculomotor drive is used to produce HR and HU movements. To address this objective, the activities of pontine burst neurons were recorded during horizontal HR and HU gaze shifts. The burst profile recorded on each HU trial was compared with the burst waveform of every HR trial obtained for the same neuron. The oculomotor drive was assumed to be comparable for the pair yielding the lowest root-mean-squared error. For matched pairs of HR and HU trials, the peak eye-in-head velocity was substantially smaller in the HU condition, and the reduction was usually greater than the peak head velocity of the HU trial. A time-varying attenuation index, defined as the difference in HR and HU eye velocity waveforms divided by head velocity [α = ( Ḣhr − Ėhu)/ Ḣ] was computed. The index was variable at the onset of the gaze shift, but it settled at values several times greater than 1. The index then decreased gradually during the movement and stabilized at 1 around the end of gaze shift. These results imply that substantial attenuation in eye velocity occurs, at least partially, downstream of the burst neurons. We speculate on the potential roles of burst-tonic neurons in the neural integrator and various cell types in the vestibular nuclei in mediating the attenuation in eye velocity in the presence of head movements.

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.

Contribution of Head Movement to Gaze Command Coding in Monkey Frontal Cortex and Superior Colliculus

2003 ◽  
Vol 90 (4) ◽  
pp. 2770-2776 ◽  
Author(s):  
Julio C. Martinez-Trujillo ◽  
Eliana M. Klier ◽  
Hongying Wang ◽  
J. Douglas Crawford
Keyword(s):  
Superior Colliculus ◽  
Neural Control ◽  
Significant Contribution ◽  
Head Movements ◽  
Vector Model ◽  
Gaze Control ◽  
Gaze Shift ◽  
Visual Model ◽  
The Gaze ◽  
Supplementary Eye Fields

Most of what we know about the neural control of gaze comes from experiments in head-fixed animals, but several “head-free” studies have suggested that fixing the head dramatically alters the apparent gaze command. We directly investigated this issue by quantitatively comparing head-fixed and head-free gaze trajectories evoked by electrically stimulating 52 sites in the superior colliculus (SC) of two monkeys and 23 sites in the supplementary eye fields (SEF) of two other monkeys. We found that head movements made a significant contribution to gaze shifts evoked from both neural structures. In the majority of the stimulated sites, average gaze amplitude was significantly larger and individual gaze trajectories were significantly less convergent in space with the head free to move. Our results are consistent with the hypothesis that head-fixed stimulation only reveals the oculomotor component of the gaze shift, not the true, planned goal of the movement. One implication of this finding is that when comparing stimulation data against popular gaze control models, freeing the head shifts the apparent coding of gaze away from a “spatial code” toward a simpler visual model in the SC and toward an eye-centered or fixed-vector model representation in the SEF.

Eye-head coordination during large gaze shifts

1995 ◽  
Vol 73 (2) ◽  
pp. 766-779 ◽  
Author(s):  
D. Tweed ◽  
B. Glenn ◽  
T. Vilis
Keyword(s):  
Degrees Of Freedom ◽  
Human Subjects ◽  
Three Dimensional ◽  
Vertical Axis ◽  
Head Movements ◽  
Gaze Shifts ◽  
Healthy Human ◽  
Vertical Movements ◽  
The Gaze ◽  
Acceleration And Deceleration

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)

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