Situating the Superior Colliculus within the Gaze Control Network

Author(s):  
Michael Platt ◽  
Brian Lau ◽  
Paul Glimcher
2003 ◽  
Vol 90 (4) ◽  
pp. 2770-2776 ◽  
Author(s):  
Julio C. Martinez-Trujillo ◽  
Eliana M. Klier ◽  
Hongying Wang ◽  
J. Douglas Crawford

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.


1998 ◽  
Vol 79 (6) ◽  
pp. 3060-3076 ◽  
Author(s):  
Martin Paré ◽  
Daniel Guitton

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.


Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 371-371
Author(s):  
R M Steinman ◽  
T I Forofonova ◽  
J Epelboim ◽  
M R Stepanov

Epelboim et al (1996 Vision Research35 3401 – 3422) reported that cyclopean gaze errors were smaller than either eye's during tapping and looking-only tasks. This raised two questions: (i) does cyclopean gaze accuracy require binocular input, and (ii) when only one eye sees, is its gaze more accurate than the patched eye's? Most oculomotorists probably expect an affirmative answer to both. Neither expectation was fulfilled. The Maryland Revolving Field Monitor recorded, with exceptional accuracy, eye movements of two unrestrained subjects tapping or only looking, in a specified order, at four randomly positioned LEDs, with monocular or binocular viewing. Subjects either tapped with their finger tips naturally, or unnaturally via a rod (2 mm diameter, 1.5 cm long), glued to a sewing thimble. Instructions were to be fast, but make no order errors. With binocular viewing, cyclopean gaze accuracy was best during looking-only. During natural tapping, gaze errors increased, becoming no smaller than success required. Both tasks were learned equally fast, but as expected, the younger subject (aged 27 years) performed ∼ 40% faster than the older subject (aged 69 years). Unnatural, monocular viewing produced odd results, eg cyclopean gaze error was smallest when only one eye could see in some conditions. Only the older subject served in the unnatural tapping task because the younger's errors were too close to his gaze control limit. The older subject, who was suitable, reduced his cyclopean gaze error by 56%, from 1.4 to 0.9 deg. These results support our claim that the gaze error allowed is adjusted to the visuomotor demands of different tasks.


2007 ◽  
Vol 98 (4) ◽  
pp. 2022-2037 ◽  
Author(s):  
Mark M. G. Walton ◽  
Bernard Bechara ◽  
Neeraj J. Gandhi

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.


Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 147-147 ◽  
Author(s):  
M Flückiger ◽  
B Baumberger

Our purpose was to show how the modification of visual information available to moving observers can change the way they perceive their path and the structure of the environments they pass through. Stimulus trials simulated locomotion across a tree-filled plane while the gaze was directed at a particular tree. In the first experiment we varied the angle between the line of gaze and the simulated direction of movement (GMA) between 0° and 20°. In the second experiment we used either inward displacement (ID) of some objects (moving towards the fovea) or other flow patterns. After each trial, participants drew their path or the position of the particular tree on a schematic map of the environment. In the first experiment, with respect to the fixation point, as GMA increased so did the shift in the drawn paths, and we measured a significant correlation between the two. In the second, ID changed the accuracy of depth representation for the most distant objects in the visual field. In conclusion, the strong relation between GMA and the reproduced paths, even though they are discrepant from the true paths, suggests that the maintenance of course in the real world may not be based on a maplike mental representation of one's trajectory. In addition, opposite motions in the same region of the visual field (as encountered with ID patterns), may significantly modify the information used for integrating spatial relationships in the environment. The attractive power of these regions in gaze control may also renew our theoretical interest in selective attention.


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