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.

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 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.

Subcortical contributions to head movements in macaques. I. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus

1994 ◽  
Vol 72 (6) ◽  
pp. 2648-2664 ◽  
Author(s):  
R. J. Cowie ◽  
D. L. Robinson
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Superior Colliculus ◽  
Head Movement ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Reticular Nucleus ◽  
Gaze Shifts ◽  
Gigantocellular Reticular Nucleus ◽  
External Events

1. These studies were initiated to understand the neural sites and mechanisms controlling head movements during gaze shifts. Gaze shifts are made by saccadic eye movements with and without head movements. Sites were stimulated electrically within the brain stem of awake, trained monkeys relatively free to make head movements to study the head-movement components of gaze shifts. 2. Electrical stimulation in and around the gigantocellular reticular nucleus evoked head movements in the ipsilateral direction. Gaze shifts were never evoked from these sites, presumably because the vestibulo-ocular reflex compensated. The rough topography of this region included large head movements laterally, small movements medially, downward movements from dorsal sites, and upward movements more ventrally. 3. The initial position of the head influenced the magnitude of the elicited movement with larger movements produced when the head was directed to the contralateral side. Attentive fixation was associated with larger and faster head movements when compared with those evoked during spontaneous behavior. 4. The superior colliculus makes a significant contribution to gaze shifts and has been shown to contribute to head movements. Because the colliculus is a major source of afferents to the gigantocellular reticular nucleus, comparable stimulation studies of the superior colliculus were conducted. When the colliculus was excited, shifts of gaze in the contralateral direction were predominant. These were most often accomplished by saccadic eye movements, however, we frequently elicited head movements that had an average latency 10 ms longer than those elicited from the reticular head movement region. Sites evoking head movements tended to be deeper and more caudal than loci eliciting eye movements. Neither the onset latencies, amplitudes, nor peak velocities of head movements and eye movements were correlated. Gaze shifts evoked from the caudal colliculus with the head free were larger than those elicited from the same site with the head fixed. 5. These studies demonstrate that both the superior colliculus and gigantocellular reticular nucleus mediate head movements. The colliculus plays a role in orienting to external events, and so collicular head movements predominantly were associated with gaze shifts, with the eye and head movements uncoupled. The medullary reticular system may play a role in the integration of a wider range of movements. Head movements from the medullary reticular sites probably participate in several forms of head movements, such as those that are related to postural reflexes, started volitionally, and/or oriented to external events.

Electrical Microstimulation of the Fastigial Oculomotor Region in the Head-Unrestrained Monkey

2009 ◽  
Vol 102 (1) ◽  
pp. 320-336 ◽  
Author(s):  
Julie Quinet ◽  
Laurent Goffart
Keyword(s):  
Neural Network ◽  
Eye Movements ◽  
Stimulation Frequency ◽  
Head Movements ◽  
Local Injection ◽  
Fastigial Nucleus ◽  
Gaze Shifts ◽  
Electrical Microstimulation ◽  
The Gaze ◽  
The Relationship

It has been shown that inactivation of the caudal fastigial nucleus (cFN) by local injection of muscimol leads to inaccurate gaze shifts in the head-unrestrained monkey and that the gaze dysmetria is primarily due to changes in the horizontal amplitude of eye saccades in the orbit. Moreover, changes in the relationship between amplitude and duration are observed for only the eye saccades and not for the head movements. These results suggest that the cFN output primarily influences a neural network involved in moving the eyes in the orbit. The present study further tested this hypothesis by examining whether head movements could be evoked by electrical microstimulation of the saccade-related region in the cFN. Long stimulation trains (200–300 ms) evoked staircase gaze shifts that were ipsi- or contralateral, depending on the stimulated site. These gaze shifts were small in amplitude and were essentially accomplished by saccadic movements of the eyes. Head movements were observed in some sites but their amplitudes were very small (mean = 2.4°). The occurrence of head movements and their amplitude were not enhanced by increasing stimulation frequency or intensity. In several cases, electrically evoked gaze shifts exhibited an eye-head coupling that was different from that observed in visually triggered gaze shifts. This study provides additional observations suggesting that the saccade-related region in the cFN modulates the generation of eye movements and that the deep cerebellar output region involved in influencing head movements is located elsewhere.

Eye-Head Coordination During Head-Unrestrained Gaze Shifts in Rhesus Monkeys

1997 ◽  
Vol 77 (5) ◽  
pp. 2328-2348 ◽  
Author(s):  
Edward G. Freedman ◽  
David L. Sparks
Keyword(s):  
Head Movement ◽  
Rhesus Monkeys ◽  
Initial Position ◽  
Head Movements ◽  
Gaze Shifts ◽  
Unit Recording ◽  
Gaze Shift ◽  
The Gaze ◽  
Two Factors ◽  
Eye Velocity

Freedman, Edward G. and David L. Sparks. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J. Neurophysiol. 77: 2328–2348, 1997. We analyzed gaze shifts made by trained rhesus monkeys with completely unrestrained heads during performance of a delayed gaze shift task. Subjects made horizontal, vertical, and oblique gaze shifts to visual targets. We found that coordinated eye-head movements are characterized by a set of lawful relationships, and that the initial position of the eyes in the orbits and the direction of the gaze shift are two factors that influence these relationships. Head movements did not contribute to the change in gaze position during small gaze shifts (<20°) directed along the horizontal meridian, when the eyes were initially centered in the orbits. For larger gaze shifts (25–90°), the head contribution to the gaze shift increased linearly with increasing gaze shift amplitude, and eye movement amplitude saturated at an asymptotic amplitude of ∼35°. When the eyes began deviated in the orbits contralateral to the direction of the ensuing gaze shift, the head contributed less and the eyes more to amplitude-matched gaze shifts. The relative timing of eye and head movements was altered by initial eye position; head latency relative to gaze onset increased as the eyes began in more contralateral initial positions. The direction of the gaze shift also affected the relative amplitudes of eye and head movements; as gaze shifts were made in progressively more vertical directions, eye amplitude increased and head contribution declined systematically. Eye velocity was a saturating function of gaze amplitude for movements without a head contribution (gaze amplitude <20°). As head contribution increased with increasing gaze amplitude (20–60°), peak eye velocity declined by >200°/s and head velocity increased by 100°/s. For constant-amplitude eye movements (∼30°), eye velocity declined as the velocity of the concurrent head movement increased. On the basis of these relationships, it is possible to accurately predict gaze amplitude, the amplitudes of the eye and head components of the gaze shift, and gaze, eye, and head velocities, durations and latencies if the two-dimensional displacement of the target and the initial position of the eyes in the orbits are known. These data indicate that signals related to the initial positions of the eyes in the orbits and the direction of the gaze shift influence separate eye and head movement commands. The hypothesis that this divergence of eye and head commands occurs downstream from the superior colliculus is supported by recent electrical stimulation and single-unit recording data.

scholarly journals Superior colliculus drives stimulus-evoked directionally biased saccades and attempted head movements in head-fixed mice

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Sebastian H Zahler ◽  
David E Taylor ◽  
Joey Y Wong ◽  
Julia M Adams ◽  
Evan H Feinberg
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Head Movement ◽  
Head Movements ◽  
Gaze Shifts ◽  
Tactile Stimuli ◽  
Vestibular Cues ◽  
Saccade Direction ◽  
Head Rotations ◽  
Prevailing View

Animals investigate their environments by directing their gaze towards salient stimuli. In the prevailing view, mouse gaze shifts entail head rotations followed by brainstem-mediated eye movements, including saccades to reset the eyes. These 'recentering' saccades are attributed to head movement-related vestibular cues. However, microstimulating mouse superior colliculus (SC) elicits directed head and eye movements resembling SC-dependent sensory-guided gaze shifts in other species, suggesting that mouse gaze shifts may be more flexible than has been recognized. We investigated this possibility by tracking eye and attempted head movements in a head-fixed preparation that eliminates head movement-related sensory cues. We found tactile stimuli evoke directionally biased saccades coincident with attempted head rotations. Differences in saccade endpoints across stimuli are associated with distinct stimulus-dependent relationships between initial eye position and saccade direction and amplitude. Optogenetic perturbations revealed SC drives these gaze shifts. Thus, head-fixed mice make sensory-guided, SC-dependent gaze shifts involving coincident, directionally biased saccades and attempted head movements. Our findings uncover flexibility in mouse gaze shifts and provide a foundation for studying head-eye coupling.

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 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 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.

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