Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts

2003 ◽  
Vol 6 (4) ◽  
pp. 404-413 ◽  
Author(s):  
André Bergeron ◽  
Satoshi Matsuo ◽  
Daniel Guitton
Keyword(s):  
Superior Colliculus ◽  
Saccade Amplitude ◽  
Gaze Shifts

Distributed spatial coding in the superior colliculus: A review

1991 ◽  
Vol 6 (1) ◽  
pp. 3-13 ◽  
Author(s):  
James T. McIlwain
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Receptive Fields ◽  
Saccadic Eye Movements ◽  
Visual Direction ◽  
Saccade Amplitude ◽  
Spatial Coding ◽  
Distributed Coding

AbstractThis paper reviews evidence that the superior colliculus (SC) of the midbrain represents visual direction and certain aspects of saccadic eye movements in the distribution of activity across a population of cells. Accurate and precise eye movements appear to be mediated, in part at least, by cells of the SC that have large sensory receptive fields and/or discharge in association with a range of saccades. This implies that visual points or saccade targets are represented by patches rather than points of activity in the SC. Perturbation of the pattern of collicular discharge by focal inactivation modifies saccade amplitude and direction in a way consistent with distributed coding. Several models have been advanced to explain how such a code might be implemented in the colliculus. Evidence related to these hypotheses is examined and continuing uncertainties are identified.

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.

Movement of neural activity on the superior colliculus motor map during gaze shifts

Science ◽  
1991 ◽  
Vol 251 (4999) ◽  
pp. 1358-1360 ◽  
Author(s):  
D. Munoz ◽  
D Pelisson ◽  
D Guitton
Keyword(s):  
Superior Colliculus ◽  
Neural Activity ◽  
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.

scholarly journals Coupling Between Horizontal and Vertical Components of Saccadic Eye Movements During Constant Amplitude and Direction Gaze Shifts in the Rhesus Monkey

2008 ◽  
Vol 100 (6) ◽  
pp. 3375-3393 ◽  
Author(s):  
Edward G. Freedman
Keyword(s):  
Eye Movements ◽  
Saccadic Eye Movements ◽  
Head Movements ◽  
Horizontal Meridian ◽  
Constant Amplitude ◽  
Saccade Amplitude ◽  
Gaze Shifts ◽  
Horizontal Saccade ◽  
Vertical Saccade ◽  
Saccade Duration

When the head is free to move, changes in the direction of the line of sight (gaze shifts) can be accomplished using coordinated movements of the eyes and head. During repeated gaze shifts between the same two targets, the amplitudes of the saccadic eye movements and movements of the head vary inversely as a function of the starting positions of the eyes in the orbits. In addition, as head-movement amplitudes and velocities increase, saccade velocities decline. Taken together these observations lead to a reversal in the expected correlation between saccade duration and amplitude: small-amplitude saccades associated with large head movements can have longer durations than larger-amplitude saccades associated with small head movements. The data in this report indicate that this reversal occurs during gaze shifts along the horizontal meridian and also when considering the horizontal component of oblique saccades made when the eyes begin deviated only along the horizontal meridian. Under these conditions, it is possible to determine whether the variability in the duration of the constant amplitude vertical component of oblique saccades is accounted for better by increases in horizontal saccade amplitude or increases in horizontal saccade duration. Results show that vertical saccade duration can be inversely related to horizontal saccade amplitude (or unrelated to it) but that horizontal saccade duration is an excellent predictor of vertical saccade duration. Modifications to existing hypotheses of gaze control are assessed based on these new observations and a mechanism is proposed that can account for these data.

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.

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